diff --git a/.changeset/lucky-walls-jog.md b/.changeset/lucky-walls-jog.md
new file mode 100644
index 00000000000..ea28730a1b7
--- /dev/null
+++ b/.changeset/lucky-walls-jog.md
@@ -0,0 +1,6 @@
+---
+"@primer/react": minor
+"@primer/styled-react": patch
+---
+
+feat: support custom slots
diff --git a/packages/react/src/ActionList/Description.tsx b/packages/react/src/ActionList/Description.tsx
index 9a9283ee567..dc21f933387 100644
--- a/packages/react/src/ActionList/Description.tsx
+++ b/packages/react/src/ActionList/Description.tsx
@@ -3,6 +3,7 @@ import Truncate from '../Truncate'
 import {ItemContext} from './shared'
 import classes from './ActionList.module.css'
 import {clsx} from 'clsx'
+import type {FCWithSlotMarker} from '../utils/types/Slots'
 
 export type ActionListDescriptionProps = {
   /**
@@ -21,7 +22,7 @@ export type ActionListDescriptionProps = {
   truncate?: boolean
 }
 
-export const Description: React.FC<React.PropsWithChildren<ActionListDescriptionProps>> = ({
+export const Description: FCWithSlotMarker<React.PropsWithChildren<ActionListDescriptionProps>> = ({
   variant = 'inline',
   className,
   truncate,
@@ -70,3 +71,5 @@ export const Description: React.FC<React.PropsWithChildren<ActionListDescription
     )
   }
 }
+
+Description.__SLOT__ = Symbol('ActionList.Description')
diff --git a/packages/react/src/ActionList/Divider.tsx b/packages/react/src/ActionList/Divider.tsx
index 09aee9fb7e3..66018ac3798 100644
--- a/packages/react/src/ActionList/Divider.tsx
+++ b/packages/react/src/ActionList/Divider.tsx
@@ -1,6 +1,7 @@
 import type React from 'react'
 import {clsx} from 'clsx'
 import classes from './ActionList.module.css'
+import type {FCWithSlotMarker} from '../utils/types/Slots'
 
 export type ActionListDividerProps = {
   className?: string
@@ -10,7 +11,7 @@ export type ActionListDividerProps = {
 /**
  * Visually separates `Items` or `Groups` in an `ActionList`.
  */
-export const Divider: React.FC<React.PropsWithChildren<ActionListDividerProps>> = ({className, style}) => {
+export const Divider: FCWithSlotMarker<React.PropsWithChildren<ActionListDividerProps>> = ({className, style}) => {
   return (
     <li
       className={clsx(className, classes.Divider)}
@@ -20,3 +21,5 @@ export const Divider: React.FC<React.PropsWithChildren<ActionListDividerProps>>
     />
   )
 }
+
+Divider.__SLOT__ = Symbol('ActionList.Divider')
diff --git a/packages/react/src/ActionList/Group.tsx b/packages/react/src/ActionList/Group.tsx
index 10fec9a3934..441e79302c9 100644
--- a/packages/react/src/ActionList/Group.tsx
+++ b/packages/react/src/ActionList/Group.tsx
@@ -7,6 +7,7 @@ import {invariant} from '../utils/invariant'
 import {clsx} from 'clsx'
 import classes from './ActionList.module.css'
 import groupClasses from './Group.module.css'
+import type {FCWithSlotMarker} from '../utils/types/Slots'
 
 type HeadingProps = {
   as?: 'h1' | 'h2' | 'h3' | 'h4' | 'h5' | 'h6'
@@ -67,7 +68,7 @@ export const GroupContext = React.createContext<ContextProps>({
   selectionVariant: undefined,
 })
 
-export const Group: React.FC<React.PropsWithChildren<ActionListGroupProps>> = ({
+export const Group: FCWithSlotMarker<React.PropsWithChildren<ActionListGroupProps>> = ({
   title,
   variant = 'subtle',
   auxiliaryText,
@@ -138,7 +139,7 @@ export type ActionListGroupHeadingProps = Pick<ActionListGroupProps, 'variant' |
  * hidden from the accessibility tree due to the limitation of listbox children. https://w3c.github.io/aria/#listbox
  * groups under menu or listbox are labelled by `aria-label`
  */
-export const GroupHeading: React.FC<React.PropsWithChildren<ActionListGroupHeadingProps>> = ({
+export const GroupHeading: FCWithSlotMarker<React.PropsWithChildren<ActionListGroupHeadingProps>> = ({
   as,
   variant = 'subtle',
   // We are not recommending this prop to be used, it should only be used internally for incremental rollout.
@@ -210,3 +211,6 @@ export const GroupHeading: React.FC<React.PropsWithChildren<ActionListGroupHeadi
 
 GroupHeading.displayName = 'ActionList.GroupHeading'
 Group.displayName = 'ActionList.Group'
+
+Group.__SLOT__ = Symbol('ActionList.Group')
+GroupHeading.__SLOT__ = Symbol('ActionList.GroupHeading')
diff --git a/packages/react/src/ActionList/Heading.tsx b/packages/react/src/ActionList/Heading.tsx
index 0d1945193ef..510c94231d8 100644
--- a/packages/react/src/ActionList/Heading.tsx
+++ b/packages/react/src/ActionList/Heading.tsx
@@ -51,3 +51,5 @@ export const Heading = forwardRef(({as, size, children, visuallyHidden = false,
 }) as PolymorphicForwardRefComponent<HeadingLevels, ActionListHeadingProps>
 
 Heading.displayName = 'ActionList.Heading'
+
+Heading.__SLOT__ = Symbol('ActionList.Heading')
diff --git a/packages/react/src/ActionList/Item.tsx b/packages/react/src/ActionList/Item.tsx
index de12e491d8c..b25a169bd50 100644
--- a/packages/react/src/ActionList/Item.tsx
+++ b/packages/react/src/ActionList/Item.tsx
@@ -314,8 +314,9 @@ const UnwrappedItem = <As extends React.ElementType = 'li'>(
   )
 }
 
-const Item = fixedForwardRef(UnwrappedItem)
-
-Object.assign(Item, {displayName: 'ActionList.Item'})
+const Item = Object.assign(fixedForwardRef(UnwrappedItem), {
+  displayName: 'ActionList.Item',
+  __SLOT__: Symbol('ActionList.Item'),
+})
 
 export {Item}
diff --git a/packages/react/src/ActionList/LinkItem.tsx b/packages/react/src/ActionList/LinkItem.tsx
index cb18077eaf0..8939b450284 100644
--- a/packages/react/src/ActionList/LinkItem.tsx
+++ b/packages/react/src/ActionList/LinkItem.tsx
@@ -56,3 +56,5 @@ export const LinkItem = React.forwardRef(
 ) as PolymorphicForwardRefComponent<'a', ActionListLinkItemProps>
 
 LinkItem.displayName = 'ActionList.LinkItem'
+
+LinkItem.__SLOT__ = Symbol('ActionList.LinkItem')
diff --git a/packages/react/src/ActionList/TrailingAction.tsx b/packages/react/src/ActionList/TrailingAction.tsx
index daa68dac8ba..933c3a6f584 100644
--- a/packages/react/src/ActionList/TrailingAction.tsx
+++ b/packages/react/src/ActionList/TrailingAction.tsx
@@ -66,3 +66,5 @@ export const TrailingAction = forwardRef(
     )
   },
 ) as PolymorphicForwardRefComponent<'button' | 'a', ActionListTrailingActionProps>
+
+TrailingAction.__SLOT__ = Symbol('ActionList.TrailingAction')
diff --git a/packages/react/src/ActionList/Visuals.tsx b/packages/react/src/ActionList/Visuals.tsx
index e93f4ebca44..c091391e465 100644
--- a/packages/react/src/ActionList/Visuals.tsx
+++ b/packages/react/src/ActionList/Visuals.tsx
@@ -5,6 +5,7 @@ import {ItemContext} from './shared'
 import {Tooltip, type TooltipProps} from '../TooltipV2'
 import {clsx} from 'clsx'
 import classes from './ActionList.module.css'
+import type {FCWithSlotMarker} from '../utils/types/Slots'
 
 export type VisualProps = React.HTMLAttributes<HTMLSpanElement>
 
@@ -13,7 +14,7 @@ export const VisualContainer: React.FC<React.PropsWithChildren<VisualProps>> = (
 }
 
 export type ActionListLeadingVisualProps = VisualProps
-export const LeadingVisual: React.FC<React.PropsWithChildren<VisualProps>> = ({className, ...props}) => {
+export const LeadingVisual: FCWithSlotMarker<React.PropsWithChildren<VisualProps>> = ({className, ...props}) => {
   return (
     <VisualContainer className={clsx(className, classes.LeadingVisual)} {...props}>
       {props.children}
@@ -22,7 +23,7 @@ export const LeadingVisual: React.FC<React.PropsWithChildren<VisualProps>> = ({c
 }
 
 export type ActionListTrailingVisualProps = VisualProps
-export const TrailingVisual: React.FC<React.PropsWithChildren<VisualProps>> = ({className, ...props}) => {
+export const TrailingVisual: FCWithSlotMarker<React.PropsWithChildren<VisualProps>> = ({className, ...props}) => {
   const {trailingVisualId} = React.useContext(ItemContext)
   return (
     <VisualContainer className={clsx(className, classes.TrailingVisual)} id={trailingVisualId} {...props}>
@@ -78,3 +79,6 @@ export const VisualOrIndicator: React.FC<
 
 LeadingVisual.displayName = 'ActionList.LeadingVisual'
 TrailingVisual.displayName = 'ActionList.TrailingVisual'
+
+LeadingVisual.__SLOT__ = Symbol('ActionList.LeadingVisual')
+TrailingVisual.__SLOT__ = Symbol('ActionList.TrailingVisual')
diff --git a/packages/react/src/ActionMenu/ActionMenu.tsx b/packages/react/src/ActionMenu/ActionMenu.tsx
index 23e0cf7e001..aa6f4ae808c 100644
--- a/packages/react/src/ActionMenu/ActionMenu.tsx
+++ b/packages/react/src/ActionMenu/ActionMenu.tsx
@@ -15,6 +15,8 @@ import type {ForwardRefComponent as PolymorphicForwardRefComponent} from '../uti
 import {Tooltip} from '../TooltipV2/Tooltip'
 import styles from './ActionMenu.module.css'
 import {useResponsiveValue, type ResponsiveValue} from '../hooks/useResponsiveValue'
+import {isSlot} from '../utils/is-slot'
+import type {FCWithSlotMarker, WithSlotMarker} from '../utils/types/Slots'
 
 export type MenuCloseHandler = (
   gesture: 'anchor-click' | 'click-outside' | 'escape' | 'tab' | 'item-select' | 'arrow-left' | 'close',
@@ -71,7 +73,7 @@ const mergeAnchorHandlers = (anchorProps: React.HTMLAttributes<HTMLElement>, but
   return mergedAnchorProps
 }
 
-const Menu: React.FC<React.PropsWithChildren<ActionMenuProps>> = ({
+const Menu: FCWithSlotMarker<React.PropsWithChildren<ActionMenuProps>> = ({
   anchorRef: externalAnchorRef,
   open,
   onOpenChange,
@@ -112,7 +114,7 @@ const Menu: React.FC<React.PropsWithChildren<ActionMenuProps>> = ({
   // 🚨 Accounting for Tooltip wrapping ActionMenu.Button or being a direct child of ActionMenu.Anchor.
   const contents = React.Children.map(children, child => {
     // Is ActionMenu.Button wrapped with Tooltip? If this is the case, our anchor is the tooltip's trigger (ActionMenu.Button's grandchild)
-    if (child.type === Tooltip) {
+    if (child.type === Tooltip || isSlot(child, Tooltip)) {
       // tooltip trigger
       const anchorChildren = child.props.children
       if (anchorChildren.type === MenuButton) {
@@ -129,7 +131,8 @@ const Menu: React.FC<React.PropsWithChildren<ActionMenuProps>> = ({
       return null
     } else if (child.type === Anchor) {
       const anchorChildren = child.props.children
-      const isWrappedWithTooltip = anchorChildren !== undefined ? anchorChildren.type === Tooltip : false
+      const isWrappedWithTooltip =
+        anchorChildren !== undefined ? anchorChildren.type === Tooltip || isSlot(anchorChildren, Tooltip) : false
       if (isWrappedWithTooltip) {
         if (anchorChildren.props.children !== null) {
           renderAnchor = anchorProps => {
@@ -175,7 +178,15 @@ const Menu: React.FC<React.PropsWithChildren<ActionMenuProps>> = ({
 }
 
 export type ActionMenuAnchorProps = {children: React.ReactElement; id?: string} & React.HTMLAttributes<HTMLElement>
-const Anchor = React.forwardRef<HTMLElement, ActionMenuAnchorProps>(({children: child, ...anchorProps}, anchorRef) => {
+const Anchor: WithSlotMarker<
+  React.ForwardRefExoticComponent<
+    {
+      children: React.ReactElement
+      id?: string
+    } & React.HTMLAttributes<HTMLElement> &
+      React.RefAttributes<HTMLElement>
+  >
+> = React.forwardRef<HTMLElement, ActionMenuAnchorProps>(({children: child, ...anchorProps}, anchorRef) => {
   const {onOpen, isSubmenu} = React.useContext(MenuContext)
 
   const openSubmenuOnRightArrow: React.KeyboardEventHandler<HTMLElement> = useCallback(
@@ -247,7 +258,7 @@ type MenuOverlayProps = Partial<OverlayProps> &
     children: React.ReactNode
     onPositionChange?: ({position}: {position: AnchorPosition}) => void
   }
-const Overlay: React.FC<React.PropsWithChildren<MenuOverlayProps>> = ({
+const Overlay: FCWithSlotMarker<React.PropsWithChildren<MenuOverlayProps>> = ({
   children,
   align = 'start',
   side,
@@ -323,4 +334,10 @@ const Overlay: React.FC<React.PropsWithChildren<MenuOverlayProps>> = ({
 }
 
 Menu.displayName = 'ActionMenu'
+
+Menu.__SLOT__ = Symbol('ActionMenu')
+MenuButton.__SLOT__ = Symbol('ActionMenu.Button')
+Anchor.__SLOT__ = Symbol('ActionMenu.Anchor')
+Overlay.__SLOT__ = Symbol('ActionMenu.Overlay')
+
 export const ActionMenu = Object.assign(Menu, {Button: MenuButton, Anchor, Overlay, Divider})
diff --git a/packages/react/src/Autocomplete/Autocomplete.tsx b/packages/react/src/Autocomplete/Autocomplete.tsx
index b5bee8299cf..993b0fcc203 100644
--- a/packages/react/src/Autocomplete/Autocomplete.tsx
+++ b/packages/react/src/Autocomplete/Autocomplete.tsx
@@ -1,6 +1,6 @@
 import type React from 'react'
 import {useCallback, useReducer, useRef} from 'react'
-import type {ComponentProps} from '../utils/types'
+import type {ComponentProps, FCWithSlotMarker} from '../utils/types'
 import {AutocompleteContext} from './AutocompleteContext'
 import AutocompleteInput from './AutocompleteInput'
 import AutocompleteMenu from './AutocompleteMenu'
@@ -46,7 +46,7 @@ const reducer = (state: State, action: Action) => {
   }
 }
 
-const Autocomplete: React.FC<React.PropsWithChildren<{id?: string}>> = ({children, id: idProp}) => {
+const Autocomplete: FCWithSlotMarker<React.PropsWithChildren<{id?: string}>> = ({children, id: idProp}) => {
   const activeDescendantRef = useRef<HTMLElement>(null)
   const scrollContainerRef = useRef<HTMLDivElement>(null)
   const inputRef = useRef<HTMLInputElement>(null)
@@ -98,6 +98,7 @@ export type {AutocompleteInputProps} from './AutocompleteInput'
 export type {AutocompleteMenuProps} from './AutocompleteMenu'
 export type {AutocompleteOverlayProps} from './AutocompleteOverlay'
 export default Object.assign(Autocomplete, {
+  __SLOT__: Symbol('Autocomplete'),
   Context: AutocompleteContext,
   Input: AutocompleteInput,
   Menu: AutocompleteMenu,
diff --git a/packages/react/src/Autocomplete/AutocompleteInput.tsx b/packages/react/src/Autocomplete/AutocompleteInput.tsx
index 270573dde08..f95c4e7f7c2 100644
--- a/packages/react/src/Autocomplete/AutocompleteInput.tsx
+++ b/packages/react/src/Autocomplete/AutocompleteInput.tsx
@@ -188,3 +188,5 @@ AutocompleteInput.displayName = 'AutocompleteInput'
 
 export type AutocompleteInputProps = ComponentProps<typeof AutocompleteInput>
 export default AutocompleteInput
+
+AutocompleteInput.__SLOT__ = Symbol('Autocomplete.Input')
diff --git a/packages/react/src/Autocomplete/AutocompleteMenu.tsx b/packages/react/src/Autocomplete/AutocompleteMenu.tsx
index d2f19b6d6f7..69918c48e99 100644
--- a/packages/react/src/Autocomplete/AutocompleteMenu.tsx
+++ b/packages/react/src/Autocomplete/AutocompleteMenu.tsx
@@ -406,3 +406,5 @@ AutocompleteMenu.displayName = 'AutocompleteMenu'
 
 export type AutocompleteMenuProps = ComponentProps<typeof AutocompleteMenu>
 export default AutocompleteMenu
+
+AutocompleteMenu.__SLOT__ = Symbol('Autocomplete.Menu')
diff --git a/packages/react/src/Autocomplete/AutocompleteOverlay.tsx b/packages/react/src/Autocomplete/AutocompleteOverlay.tsx
index caaa9279f27..d72494a7545 100644
--- a/packages/react/src/Autocomplete/AutocompleteOverlay.tsx
+++ b/packages/react/src/Autocomplete/AutocompleteOverlay.tsx
@@ -79,3 +79,5 @@ AutocompleteOverlay.displayName = 'AutocompleteOverlay'
 
 export type AutocompleteOverlayProps = ComponentProps<typeof AutocompleteOverlay>
 export default AutocompleteOverlay
+
+AutocompleteOverlay.__SLOT__ = Symbol('Autocomplete.Overlay')
diff --git a/packages/react/src/Button/Button.tsx b/packages/react/src/Button/Button.tsx
index fddc8f84aab..9019ba071a1 100644
--- a/packages/react/src/Button/Button.tsx
+++ b/packages/react/src/Button/Button.tsx
@@ -90,4 +90,6 @@ export function generateCustomSxProp(
 
 ButtonComponent.displayName = 'Button'
 
+ButtonComponent.__SLOT__ = Symbol('Button')
+
 export {ButtonComponent}
diff --git a/packages/react/src/Checkbox/Checkbox.tsx b/packages/react/src/Checkbox/Checkbox.tsx
index 6b05d5203ac..fe593f0ac45 100644
--- a/packages/react/src/Checkbox/Checkbox.tsx
+++ b/packages/react/src/Checkbox/Checkbox.tsx
@@ -6,6 +6,7 @@ import type {FormValidationStatus} from '../utils/types/FormValidationStatus'
 import {CheckboxGroupContext} from '../CheckboxGroup/CheckboxGroupContext'
 import classes from './Checkbox.module.css'
 import sharedClasses from './shared.module.css'
+import type {WithSlotMarker} from '../utils/types'
 
 export type CheckboxProps = {
   /**
@@ -89,5 +90,6 @@ const Checkbox = React.forwardRef<HTMLInputElement, CheckboxProps>(
 )
 
 Checkbox.displayName = 'Checkbox'
+;(Checkbox as WithSlotMarker<typeof Checkbox>).__SLOT__ = Symbol('Checkbox')
 
-export default Checkbox
+export default Checkbox as WithSlotMarker<typeof Checkbox>
diff --git a/packages/react/src/CheckboxGroup/CheckboxGroup.tsx b/packages/react/src/CheckboxGroup/CheckboxGroup.tsx
index 30c4fb9b6d3..fd064c7973c 100644
--- a/packages/react/src/CheckboxGroup/CheckboxGroup.tsx
+++ b/packages/react/src/CheckboxGroup/CheckboxGroup.tsx
@@ -1,4 +1,4 @@
-import type {ChangeEvent, ChangeEventHandler, FC} from 'react'
+import type {ChangeEvent, ChangeEventHandler} from 'react'
 import React from 'react'
 import type {CheckboxOrRadioGroupProps} from '../internal/components/CheckboxOrRadioGroup'
 import CheckboxOrRadioGroup from '../internal/components/CheckboxOrRadioGroup'
@@ -9,6 +9,8 @@ import {useRenderForcingRef} from '../hooks'
 import FormControl from '../FormControl'
 import Checkbox from '../Checkbox/Checkbox'
 import {CheckboxGroupContext} from './CheckboxGroupContext'
+import {isSlot} from '../utils/is-slot'
+import type {FCWithSlotMarker} from '../utils/types'
 
 export type CheckboxGroupProps = {
   /**
@@ -17,16 +19,21 @@ export type CheckboxGroupProps = {
   onChange?: (selected: string[], e?: ChangeEvent<HTMLInputElement>) => void
 } & CheckboxOrRadioGroupProps
 
-const CheckboxGroup: FC<React.PropsWithChildren<CheckboxGroupProps>> = ({children, disabled, onChange, ...rest}) => {
+const CheckboxGroup: FCWithSlotMarker<React.PropsWithChildren<CheckboxGroupProps>> = ({
+  children,
+  disabled,
+  onChange,
+  ...rest
+}) => {
   const formControlComponentChildren = React.Children.toArray(children)
-    .filter(child => React.isValidElement(child) && child.type === FormControl)
+    .filter(child => React.isValidElement(child) && (child.type === FormControl || isSlot(child, FormControl)))
     .map(formControlComponent =>
       React.isValidElement(formControlComponent) ? formControlComponent.props.children : [],
     )
     .flat()
 
   const checkedCheckboxes = React.Children.toArray(formControlComponentChildren)
-    .filter(child => React.isValidElement(child) && child.type === Checkbox)
+    .filter(child => React.isValidElement(child) && (child.type === Checkbox || isSlot(child, Checkbox)))
     .map(
       checkbox =>
         React.isValidElement(checkbox) &&
@@ -73,3 +80,5 @@ export default Object.assign(CheckboxGroup, {
   Label: CheckboxOrRadioGroupLabel,
   Validation: CheckboxOrRadioGroupValidation,
 })
+
+CheckboxGroup.__SLOT__ = Symbol('CheckboxGroup')
diff --git a/packages/react/src/FormControl/FormControl.tsx b/packages/react/src/FormControl/FormControl.tsx
index 8dea4aadb0d..7a7e3353ff1 100644
--- a/packages/react/src/FormControl/FormControl.tsx
+++ b/packages/react/src/FormControl/FormControl.tsx
@@ -21,6 +21,7 @@ import {FormControlContextProvider} from './_FormControlContext'
 import {warning} from '../utils/warning'
 import classes from './FormControl.module.css'
 import {BoxWithFallback} from '../internal/components/BoxWithFallback'
+import {isSlot} from '../utils/is-slot'
 
 export type FormControlProps = {
   children?: React.ReactNode
@@ -70,12 +71,20 @@ const FormControl = React.forwardRef<HTMLDivElement, FormControlProps>(
     const captionId = slots.caption ? `${id}-caption` : undefined
     const validationStatus = slots.validation?.props.variant
     const InputComponent = childrenWithoutSlots.find(child =>
-      expectedInputComponents.some(inputComponent => React.isValidElement(child) && child.type === inputComponent),
+      expectedInputComponents.some(
+        inputComponent =>
+          React.isValidElement(child) && (child.type === inputComponent || isSlot(child, inputComponent)),
+      ),
     )
     const inputProps = React.isValidElement(InputComponent) && InputComponent.props
     const isChoiceInput =
-      React.isValidElement(InputComponent) && (InputComponent.type === Checkbox || InputComponent.type === Radio)
-    const isRadioInput = React.isValidElement(InputComponent) && InputComponent.type === Radio
+      React.isValidElement(InputComponent) &&
+      (InputComponent.type === Checkbox ||
+        InputComponent.type === Radio ||
+        isSlot(InputComponent, Checkbox) ||
+        isSlot(InputComponent, Radio))
+    const isRadioInput =
+      React.isValidElement(InputComponent) && (InputComponent.type === Radio || isSlot(InputComponent, Radio))
 
     if (InputComponent) {
       warning(
@@ -139,7 +148,8 @@ const FormControl = React.forwardRef<HTMLDivElement, FormControlProps>(
             : null}
           {childrenWithoutSlots.filter(
             child =>
-              React.isValidElement(child) && ![Checkbox, Radio].some(inputComponent => child.type === inputComponent),
+              React.isValidElement(child) &&
+              ![Checkbox, Radio].some(inputComponent => child.type === inputComponent || isSlot(child, inputComponent)),
           )}
         </div>
         {slots.leadingVisual ? (
@@ -204,7 +214,9 @@ const FormControl = React.forwardRef<HTMLDivElement, FormControlProps>(
             {childrenWithoutSlots.filter(
               child =>
                 React.isValidElement(child) &&
-                !expectedInputComponents.some(inputComponent => child.type === inputComponent),
+                !expectedInputComponents.some(
+                  inputComponent => child.type === inputComponent || isSlot(child, inputComponent),
+                ),
             )}
             {slots.validation ? (
               <ValidationAnimationContainer show>{slots.validation}</ValidationAnimationContainer>
@@ -218,6 +230,7 @@ const FormControl = React.forwardRef<HTMLDivElement, FormControlProps>(
 )
 
 export default Object.assign(FormControl, {
+  __SLOT__: Symbol('FormControl'),
   Caption: FormControlCaption,
   Label: FormControlLabel,
   LeadingVisual: FormControlLeadingVisual,
diff --git a/packages/react/src/FormControl/FormControlCaption.tsx b/packages/react/src/FormControl/FormControlCaption.tsx
index 292200fea73..56a9cdeeff7 100644
--- a/packages/react/src/FormControl/FormControlCaption.tsx
+++ b/packages/react/src/FormControl/FormControlCaption.tsx
@@ -31,4 +31,6 @@ function FormControlCaption({id, children, sx, className, style}: FormControlCap
   )
 }
 
+FormControlCaption.__SLOT__ = Symbol('FormControl.Caption')
+
 export {FormControlCaption}
diff --git a/packages/react/src/FormControl/FormControlLabel.tsx b/packages/react/src/FormControl/FormControlLabel.tsx
index ff2a3ffe97c..272736759b4 100644
--- a/packages/react/src/FormControl/FormControlLabel.tsx
+++ b/packages/react/src/FormControl/FormControlLabel.tsx
@@ -2,6 +2,7 @@ import type React from 'react'
 import type {SxProp} from '../sx'
 import {useFormControlContext} from './_FormControlContext'
 import {InputLabel} from '../internal/components/InputLabel'
+import type {FCWithSlotMarker} from '../utils/types'
 
 export type Props = {
   /**
@@ -15,7 +16,7 @@ export type Props = {
   style?: React.CSSProperties
 } & SxProp
 
-const FormControlLabel: React.FC<
+const FormControlLabel: FCWithSlotMarker<
   React.PropsWithChildren<{htmlFor?: string} & React.ComponentProps<typeof InputLabel> & Props>
 > = ({as, children, htmlFor, id, visuallyHidden, requiredIndicator = true, requiredText, sx, className, ...props}) => {
   const {disabled, id: formControlId, required} = useFormControlContext()
@@ -54,4 +55,6 @@ const FormControlLabel: React.FC<
   return <InputLabel {...labelProps}>{children}</InputLabel>
 }
 
+FormControlLabel.__SLOT__ = Symbol('FormControl.Label')
+
 export default FormControlLabel
diff --git a/packages/react/src/FormControl/FormControlLeadingVisual.tsx b/packages/react/src/FormControl/FormControlLeadingVisual.tsx
index 8f29d2fc6d4..5042a344788 100644
--- a/packages/react/src/FormControl/FormControlLeadingVisual.tsx
+++ b/packages/react/src/FormControl/FormControlLeadingVisual.tsx
@@ -3,8 +3,9 @@ import type {SxProp} from '../sx'
 import {useFormControlContext} from './_FormControlContext'
 import styled from 'styled-components'
 import sx from '../sx'
+import type {FCWithSlotMarker} from '../utils/types'
 
-const FormControlLeadingVisual: React.FC<React.PropsWithChildren<SxProp & {style?: React.CSSProperties}>> = ({
+const FormControlLeadingVisual: FCWithSlotMarker<React.PropsWithChildren<SxProp & {style?: React.CSSProperties}>> = ({
   children,
   sx,
   style,
@@ -47,4 +48,6 @@ const StyledLeadingVisual = styled.div`
   ${sx}
 `
 
+FormControlLeadingVisual.__SLOT__ = Symbol('FormControl.LeadingVisual')
+
 export default FormControlLeadingVisual
diff --git a/packages/react/src/FormControl/_FormControlValidation.tsx b/packages/react/src/FormControl/_FormControlValidation.tsx
index 6678eaf8153..3268964b644 100644
--- a/packages/react/src/FormControl/_FormControlValidation.tsx
+++ b/packages/react/src/FormControl/_FormControlValidation.tsx
@@ -3,6 +3,7 @@ import InputValidation from '../internal/components/InputValidation'
 import type {SxProp} from '../sx'
 import type {FormValidationStatus} from '../utils/types/FormValidationStatus'
 import {useFormControlContext} from './_FormControlContext'
+import type {FCWithSlotMarker} from '../utils/types'
 
 export type FormControlValidationProps = {
   variant: FormValidationStatus
@@ -11,7 +12,7 @@ export type FormControlValidationProps = {
   style?: React.CSSProperties
 } & SxProp
 
-const FormControlValidation: React.FC<React.PropsWithChildren<FormControlValidationProps>> = ({
+const FormControlValidation: FCWithSlotMarker<React.PropsWithChildren<FormControlValidationProps>> = ({
   children,
   className,
   variant,
@@ -33,4 +34,6 @@ const FormControlValidation: React.FC<React.PropsWithChildren<FormControlValidat
   )
 }
 
+FormControlValidation.__SLOT__ = Symbol('FormControl.Validation')
+
 export default FormControlValidation
diff --git a/packages/react/src/FormControl/__tests__/FormControl.test.tsx b/packages/react/src/FormControl/__tests__/FormControl.test.tsx
index 3149faf4efd..d4945316e16 100644
--- a/packages/react/src/FormControl/__tests__/FormControl.test.tsx
+++ b/packages/react/src/FormControl/__tests__/FormControl.test.tsx
@@ -10,11 +10,49 @@ import Textarea from '../../Textarea'
 import TextInput from '../../TextInput'
 import TextInputWithTokens from '../../TextInputWithTokens'
 import {MarkGithubIcon} from '@primer/octicons-react'
+import type {FCWithSlotMarker} from '../../utils/types'
 
 const LABEL_TEXT = 'Form control'
 const CAPTION_TEXT = 'Hint text'
 const ERROR_TEXT = 'This field is invalid'
 
+const WrappedLabelComponent: FCWithSlotMarker<object> = () => (
+  <div>
+    {/* eslint-disable-next-line primer-react/direct-slot-children */}
+    <FormControl.Label>{LABEL_TEXT}</FormControl.Label>
+  </div>
+)
+
+WrappedLabelComponent.__SLOT__ = FormControl.Label.__SLOT__
+
+const WrappedCaptionComponent: FCWithSlotMarker<object> = () => (
+  <div>
+    {/* eslint-disable-next-line primer-react/direct-slot-children */}
+    <FormControl.Caption>{CAPTION_TEXT}</FormControl.Caption>
+  </div>
+)
+
+WrappedCaptionComponent.__SLOT__ = FormControl.Caption.__SLOT__
+
+const WrappedLeadingVisualComponent = () => (
+  <div>
+    {/* eslint-disable-next-line primer-react/direct-slot-children */}
+    <FormControl.LeadingVisual>
+      <MarkGithubIcon aria-label="Icon label" />
+    </FormControl.LeadingVisual>
+  </div>
+)
+
+WrappedLeadingVisualComponent.__SLOT__ = FormControl.LeadingVisual.__SLOT__
+
+const WrappedValidationComponent: FCWithSlotMarker<object> = () => (
+  <div>
+    <FormControl.Validation variant="error">{ERROR_TEXT}</FormControl.Validation>
+  </div>
+)
+
+WrappedValidationComponent.__SLOT__ = FormControl.Validation.__SLOT__
+
 describe('FormControl', () => {
   describe('vertically stacked layout (default)', () => {
     describe('rendering', () => {
@@ -326,6 +364,107 @@ describe('FormControl', () => {
         spy.mockRestore()
       })
     })
+
+    describe('slot identification', () => {
+      it('should correctly identify a label wrapped in a div using __SLOT__ property', () => {
+        const spy = vi.spyOn(console, 'error').mockImplementationOnce(() => {})
+
+        const {container, getByLabelText} = render(
+          <FormControl>
+            <WrappedLabelComponent />
+            <TextInput />
+          </FormControl>,
+        )
+
+        // The label should be found as a slot because of the __SLOT__ property
+        // This should NOT trigger the error about missing FormControl.Label
+        expect(spy).toHaveBeenCalledTimes(0)
+
+        // The label should function properly - input should be labeled correctly
+        const input = getByLabelText(LABEL_TEXT)
+        expect(input).toBeDefined()
+        expect(container.textContent).toContain(LABEL_TEXT)
+
+        spy.mockRestore()
+      })
+
+      it('should correctly identify a caption wrapped in a div using __SLOT__ property', () => {
+        const {container} = render(
+          <FormControl id="test-caption">
+            <FormControl.Label>{LABEL_TEXT}</FormControl.Label>
+            <TextInput />
+            <WrappedCaptionComponent />
+          </FormControl>,
+        )
+
+        // The caption should be found as a slot because of the __SLOT__ property
+        // We can verify this by checking that aria-describedby includes the caption ID
+        const input = container.querySelector('input')
+        const ariaDescribedBy = input?.getAttribute('aria-describedby') || ''
+        expect(ariaDescribedBy).toContain('test-caption-caption')
+
+        // The caption text should be rendered and functional
+        expect(container.textContent).toContain(CAPTION_TEXT)
+      })
+
+      it('should correctly identify a validation wrapped in a div using __SLOT__ property', () => {
+        const {container} = render(
+          <FormControl id="test-validation">
+            <FormControl.Label>{LABEL_TEXT}</FormControl.Label>
+            <TextInput />
+            <WrappedValidationComponent />
+          </FormControl>,
+        )
+
+        // The validation should be found as a slot because of the __SLOT__ property
+        // We can verify this by checking that aria-describedby includes the validation ID
+        const input = container.querySelector('input')
+        const ariaDescribedBy = input?.getAttribute('aria-describedby') || ''
+        expect(ariaDescribedBy).toContain('test-validation-validationMessage')
+
+        // The validation text should be rendered and functional
+        expect(container.textContent).toContain(ERROR_TEXT)
+      })
+
+      it('should correctly identify a leading visual wrapped in a div using __SLOT__ property for non-choice inputs', () => {
+        const spy = vi.spyOn(console, 'warn').mockImplementationOnce(() => {})
+
+        const {container} = render(
+          <FormControl>
+            <FormControl.Label>{LABEL_TEXT}</FormControl.Label>
+            <TextInput />
+            <WrappedLeadingVisualComponent />
+          </FormControl>,
+        )
+
+        // The leading visual should be found as a slot because of the __SLOT__ property
+        // This should trigger a warning since leading visuals are only for choice inputs
+        expect(spy).toHaveBeenCalledTimes(1)
+
+        // The icon should be rendered in the DOM
+        expect(container.querySelector('svg')).toBeDefined()
+
+        spy.mockRestore()
+      })
+      it('should correctly identify a leading visual wrapped in a div using __SLOT__ property for choice inputs', () => {
+        const {container, getByLabelText} = render(
+          <FormControl>
+            <FormControl.Label>{LABEL_TEXT}</FormControl.Label>
+            <Checkbox />
+            <WrappedLeadingVisualComponent />
+          </FormControl>,
+        )
+
+        // The leading visual should be found as a slot because of the __SLOT__ property
+        // We can verify this by checking that the leading visual container is present
+        const leadingVisualContainer = container.querySelector('[data-has-leading-visual]')
+        expect(leadingVisualContainer).toBeDefined()
+
+        // The icon should be rendered and functional
+        expect(getByLabelText('Icon label')).toBeDefined()
+        expect(container.querySelector('svg')).toBeDefined()
+      })
+    })
   })
 
   describe('checkbox and radio layout', () => {
diff --git a/packages/react/src/NavList/NavList.tsx b/packages/react/src/NavList/NavList.tsx
index 282bdae1e75..6df851846b8 100644
--- a/packages/react/src/NavList/NavList.tsx
+++ b/packages/react/src/NavList/NavList.tsx
@@ -17,6 +17,7 @@ import useIsomorphicLayoutEffect from '../utils/useIsomorphicLayoutEffect'
 import classes from '../ActionList/ActionList.module.css'
 import navListClasses from './NavList.module.css'
 import {flushSync} from 'react-dom'
+import {isSlot} from '../utils/is-slot'
 
 // ----------------------------------------------------------------------------
 // NavList
@@ -57,7 +58,9 @@ const Item = React.forwardRef<HTMLAnchorElement, NavListItemProps>(
     const {depth} = React.useContext(SubNavContext)
 
     // Get SubNav from children
-    const subNav = React.Children.toArray(children).find(child => isValidElement(child) && child.type === SubNav)
+    const subNav = React.Children.toArray(children).find(
+      child => isValidElement(child) && (child.type === SubNav || isSlot(child, SubNav)),
+    )
 
     // Get children without SubNav or TrailingAction
     const childrenWithoutSubNavOrTrailingAction = React.Children.toArray(children).filter(child =>
diff --git a/packages/react/src/PageLayout/PageLayout.tsx b/packages/react/src/PageLayout/PageLayout.tsx
index 4fc12fe3805..8d8ae16fbfd 100644
--- a/packages/react/src/PageLayout/PageLayout.tsx
+++ b/packages/react/src/PageLayout/PageLayout.tsx
@@ -10,6 +10,7 @@ import {useOverflow} from '../hooks/useOverflow'
 import {warning} from '../utils/warning'
 
 import classes from './PageLayout.module.css'
+import type {FCWithSlotMarker, WithSlotMarker} from '../utils/types'
 
 const REGION_ORDER = {
   header: 0,
@@ -338,7 +339,7 @@ export type PageLayoutHeaderProps = {
   style?: React.CSSProperties
 }
 
-const Header: React.FC<React.PropsWithChildren<PageLayoutHeaderProps>> = ({
+const Header: FCWithSlotMarker<React.PropsWithChildren<PageLayoutHeaderProps>> = ({
   'aria-label': label,
   'aria-labelledby': labelledBy,
   padding = 'none',
@@ -432,7 +433,7 @@ const contentWidths = {
   xlarge: '1280px',
 }
 
-const Content: React.FC<React.PropsWithChildren<PageLayoutContentProps>> = ({
+const Content: FCWithSlotMarker<React.PropsWithChildren<PageLayoutContentProps>> = ({
   as = 'main',
   'aria-label': label,
   'aria-labelledby': labelledBy,
@@ -781,7 +782,7 @@ export type PageLayoutFooterProps = {
   style?: React.CSSProperties
 }
 
-const Footer: React.FC<React.PropsWithChildren<PageLayoutFooterProps>> = ({
+const Footer: FCWithSlotMarker<React.PropsWithChildren<PageLayoutFooterProps>> = ({
   'aria-label': label,
   'aria-labelledby': labelledBy,
   padding = 'none',
@@ -844,8 +845,14 @@ Footer.displayName = 'PageLayout.Footer'
 // Export
 
 export const PageLayout = Object.assign(Root, {
+  __SLOT__: Symbol('PageLayout'),
   Header,
   Content,
-  Pane,
+  Pane: Pane as WithSlotMarker<typeof Pane>,
   Footer,
 })
+
+Header.__SLOT__ = Symbol('PageLayout.Header')
+Content.__SLOT__ = Symbol('PageLayout.Content')
+;(Pane as WithSlotMarker<typeof Pane>).__SLOT__ = Symbol('PageLayout.Pane')
+Footer.__SLOT__ = Symbol('PageLayout.Footer')
diff --git a/packages/react/src/Radio/Radio.tsx b/packages/react/src/Radio/Radio.tsx
index a7666aa79ed..16a98b94a53 100644
--- a/packages/react/src/Radio/Radio.tsx
+++ b/packages/react/src/Radio/Radio.tsx
@@ -4,6 +4,7 @@ import {RadioGroupContext} from '../RadioGroup/RadioGroup'
 import {clsx} from 'clsx'
 import sharedClasses from '../Checkbox/shared.module.css'
 import classes from './Radio.module.css'
+import type {WithSlotMarker} from '../utils/types'
 
 export type RadioProps = {
   /**
@@ -84,5 +85,6 @@ const Radio = React.forwardRef<HTMLInputElement, RadioProps>(
 )
 
 Radio.displayName = 'Radio'
+;(Radio as WithSlotMarker<typeof Radio>).__SLOT__ = Symbol('Radio')
 
-export default Radio
+export default Radio as WithSlotMarker<typeof Radio>
diff --git a/packages/react/src/RadioGroup/RadioGroup.tsx b/packages/react/src/RadioGroup/RadioGroup.tsx
index cc9b64b78b0..11c5fe54016 100644
--- a/packages/react/src/RadioGroup/RadioGroup.tsx
+++ b/packages/react/src/RadioGroup/RadioGroup.tsx
@@ -58,7 +58,12 @@ const RadioGroup: FC<React.PropsWithChildren<RadioGroupProps>> = ({children, dis
 }
 
 export default Object.assign(RadioGroup, {
+  __SLOT__: Symbol('RadioGroup'),
   Caption: CheckboxOrRadioGroupCaption,
   Label: CheckboxOrRadioGroupLabel,
   Validation: CheckboxOrRadioGroupValidation,
 })
+
+CheckboxOrRadioGroupCaption.__SLOT__ = Symbol('RadioGroup.Caption')
+CheckboxOrRadioGroupLabel.__SLOT__ = Symbol('RadioGroup.Label')
+CheckboxOrRadioGroupValidation.__SLOT__ = Symbol('RadioGroup.Validation')
diff --git a/packages/react/src/SegmentedControl/SegmentedControl.tsx b/packages/react/src/SegmentedControl/SegmentedControl.tsx
index b7cb8760152..f613ae4f00a 100644
--- a/packages/react/src/SegmentedControl/SegmentedControl.tsx
+++ b/packages/react/src/SegmentedControl/SegmentedControl.tsx
@@ -11,6 +11,7 @@ import type {WidthOnlyViewportRangeKeys} from '../utils/types/ViewportRangeKeys'
 import {isElement} from 'react-is'
 import classes from './SegmentedControl.module.css'
 import {clsx} from 'clsx'
+import {isSlot} from '../utils/is-slot'
 
 export type SegmentedControlProps = {
   'aria-label'?: string
@@ -63,7 +64,7 @@ const Root: React.FC<React.PropsWithChildren<SegmentedControlProps>> = ({
   const getChildIcon = (childArg: React.ReactNode): React.ReactElement | null => {
     if (
       React.isValidElement<SegmentedControlButtonProps>(childArg) &&
-      childArg.type === Button &&
+      (childArg.type === Button || isSlot(childArg, Button)) &&
       childArg.props.leadingIcon
     ) {
       if (isElement(childArg.props.leadingIcon)) {
@@ -76,7 +77,7 @@ const Root: React.FC<React.PropsWithChildren<SegmentedControlProps>> = ({
 
     if (
       React.isValidElement<SegmentedControlIconButtonProps>(childArg) &&
-      childArg.type === SegmentedControlIconButton
+      (childArg.type === SegmentedControlIconButton || isSlot(childArg, SegmentedControlIconButton))
     ) {
       if (isElement(childArg.props.icon)) {
         childArg.props.icon
@@ -183,7 +184,7 @@ const Root: React.FC<React.PropsWithChildren<SegmentedControlProps>> = ({
         if (
           responsiveVariant === 'hideLabels' &&
           React.isValidElement<SegmentedControlButtonProps>(child) &&
-          child.type === Button
+          (child.type === Button || isSlot(child, Button))
         ) {
           const {
             'aria-label': childAriaLabel,
@@ -218,6 +219,7 @@ const Root: React.FC<React.PropsWithChildren<SegmentedControlProps>> = ({
 Root.displayName = 'SegmentedControl'
 
 export const SegmentedControl = Object.assign(Root, {
+  __SLOT__: Symbol('SegmentedControl'),
   Button,
   IconButton: SegmentedControlIconButton,
 })
diff --git a/packages/react/src/SegmentedControl/SegmentedControlButton.tsx b/packages/react/src/SegmentedControl/SegmentedControlButton.tsx
index 76198ac823d..4681428ece8 100644
--- a/packages/react/src/SegmentedControl/SegmentedControlButton.tsx
+++ b/packages/react/src/SegmentedControl/SegmentedControlButton.tsx
@@ -6,6 +6,7 @@ import {isElement} from 'react-is'
 import classes from './SegmentedControl.module.css'
 import {clsx} from 'clsx'
 import CounterLabel from '../CounterLabel'
+import type {FCWithSlotMarker} from '../utils/types'
 
 export type SegmentedControlButtonProps = {
   /** The visible label rendered in the button */
@@ -20,7 +21,7 @@ export type SegmentedControlButtonProps = {
   count?: number | string
 } & ButtonHTMLAttributes<HTMLButtonElement | HTMLLIElement>
 
-const SegmentedControlButton: React.FC<React.PropsWithChildren<SegmentedControlButtonProps>> = ({
+const SegmentedControlButton: FCWithSlotMarker<React.PropsWithChildren<SegmentedControlButtonProps>> = ({
   children,
   leadingIcon: LeadingIcon,
   selected,
@@ -52,3 +53,5 @@ const SegmentedControlButton: React.FC<React.PropsWithChildren<SegmentedControlB
 }
 
 export default SegmentedControlButton
+
+SegmentedControlButton.__SLOT__ = Symbol('SegmentedControl.Button')
diff --git a/packages/react/src/SegmentedControl/SegmentedControlIconButton.tsx b/packages/react/src/SegmentedControl/SegmentedControlIconButton.tsx
index 446ebc4d4ee..ee70b240efd 100644
--- a/packages/react/src/SegmentedControl/SegmentedControlIconButton.tsx
+++ b/packages/react/src/SegmentedControl/SegmentedControlIconButton.tsx
@@ -7,6 +7,7 @@ import type {TooltipDirection} from '../TooltipV2'
 import classes from './SegmentedControl.module.css'
 import {clsx} from 'clsx'
 import {Tooltip} from '../TooltipV2'
+import type {FCWithSlotMarker} from '../utils/types'
 
 export type SegmentedControlIconButtonProps = {
   'aria-label': string
@@ -22,7 +23,7 @@ export type SegmentedControlIconButtonProps = {
   tooltipDirection?: TooltipDirection
 } & ButtonHTMLAttributes<HTMLButtonElement | HTMLLIElement>
 
-export const SegmentedControlIconButton: React.FC<React.PropsWithChildren<SegmentedControlIconButtonProps>> = ({
+export const SegmentedControlIconButton: FCWithSlotMarker<React.PropsWithChildren<SegmentedControlIconButtonProps>> = ({
   'aria-label': ariaLabel,
   icon: Icon,
   selected,
@@ -73,4 +74,6 @@ export const SegmentedControlIconButton: React.FC<React.PropsWithChildren<Segmen
   }
 }
 
+SegmentedControlIconButton.__SLOT__ = Symbol('SegmentedControl.IconButton')
+
 export default SegmentedControlIconButton
diff --git a/packages/react/src/Select/Select.tsx b/packages/react/src/Select/Select.tsx
index ad5b2fec98f..b85b33e7a0f 100644
--- a/packages/react/src/Select/Select.tsx
+++ b/packages/react/src/Select/Select.tsx
@@ -88,6 +88,7 @@ const OptGroup: React.FC<React.PropsWithChildren<React.HTMLProps<HTMLOptGroupEle
 )
 
 export default Object.assign(Select, {
+  __SLOT__: Symbol('Select'),
   Option,
   OptGroup,
 })
diff --git a/packages/react/src/SelectPanel/SelectPanel.tsx b/packages/react/src/SelectPanel/SelectPanel.tsx
index 0bc994590c7..7aa5fef65ce 100644
--- a/packages/react/src/SelectPanel/SelectPanel.tsx
+++ b/packages/react/src/SelectPanel/SelectPanel.tsx
@@ -962,6 +962,7 @@ const SecondaryLink: React.FC<LinkButtonProps & ButtonProps> = props => {
 }
 
 export const SelectPanel = Object.assign(Panel, {
+  __SLOT__: Symbol('SelectPanel'),
   SecondaryActionButton: SecondaryButton,
   SecondaryActionLink: SecondaryLink,
 })
diff --git a/packages/react/src/SubNav/SubNav.tsx b/packages/react/src/SubNav/SubNav.tsx
index 6976fb1f104..54b56942ad6 100644
--- a/packages/react/src/SubNav/SubNav.tsx
+++ b/packages/react/src/SubNav/SubNav.tsx
@@ -3,6 +3,7 @@ import type {To} from 'history'
 import React from 'react'
 
 import styles from './SubNav.module.css'
+import type {WithSlotMarker} from '../utils/types'
 
 export type SubNavProps = React.ComponentProps<'nav'> & {
   actions?: React.ReactNode
@@ -57,4 +58,9 @@ const SubNavLink = React.forwardRef<HTMLAnchorElement, SubNavLinkProps>(
 
 SubNavLink.displayName = 'SubNav.Link'
 
-export default Object.assign(SubNav, {Link: SubNavLink, Links: SubNavLinks})
+export default Object.assign(SubNav, {
+  Link: SubNavLink as WithSlotMarker<typeof SubNavLink>,
+  Links: SubNavLinks,
+  __SLOT__: Symbol('SubNav'),
+})
+;(SubNavLink as WithSlotMarker<typeof SubNavLink>).__SLOT__ = Symbol('SubNav.Link')
diff --git a/packages/react/src/TextInput/TextInput.tsx b/packages/react/src/TextInput/TextInput.tsx
index a1bd78a6ee3..ff666c81c7f 100644
--- a/packages/react/src/TextInput/TextInput.tsx
+++ b/packages/react/src/TextInput/TextInput.tsx
@@ -194,5 +194,6 @@ const TextInput = React.forwardRef<HTMLInputElement, TextInputProps>(
 TextInput.displayName = 'TextInput'
 
 export default Object.assign(TextInput, {
+  __SLOT__: Symbol('TextInput'),
   Action: TextInputAction,
 })
diff --git a/packages/react/src/TextInputWithTokens/TextInputWithTokens.tsx b/packages/react/src/TextInputWithTokens/TextInputWithTokens.tsx
index 01b89d24554..db3e65f3479 100644
--- a/packages/react/src/TextInputWithTokens/TextInputWithTokens.tsx
+++ b/packages/react/src/TextInputWithTokens/TextInputWithTokens.tsx
@@ -17,6 +17,7 @@ import UnstyledTextInput from '../internal/components/UnstyledTextInput'
 import TextInputInnerVisualSlot from '../internal/components/TextInputInnerVisualSlot'
 import styles from './TextInputWithTokens.module.css'
 import {clsx} from 'clsx'
+import type {WithSlotMarker} from '../utils/types'
 
 // eslint-disable-next-line @typescript-eslint/no-explicit-any
 type AnyReactComponent = React.ComponentType<React.PropsWithChildren<any>>
@@ -336,8 +337,9 @@ function TextInputWithTokensInnerComponent<TokenComponentType extends AnyReactCo
 const TextInputWithTokens = React.forwardRef(TextInputWithTokensInnerComponent)
 
 TextInputWithTokens.displayName = 'TextInputWithTokens'
+;(TextInputWithTokens as WithSlotMarker<typeof TextInputWithTokens>).__SLOT__ = Symbol('TextInputWithTokens')
 
 /**
  * @deprecated
  */
-export default TextInputWithTokens
+export default TextInputWithTokens as WithSlotMarker<typeof TextInputWithTokens>
diff --git a/packages/react/src/Textarea/Textarea.tsx b/packages/react/src/Textarea/Textarea.tsx
index 6cabcd57f01..f4620fc8773 100644
--- a/packages/react/src/Textarea/Textarea.tsx
+++ b/packages/react/src/Textarea/Textarea.tsx
@@ -4,6 +4,7 @@ import {TextInputBaseWrapper} from '../internal/components/TextInputWrapper'
 import type {FormValidationStatus} from '../utils/types/FormValidationStatus'
 import type {SxProp} from '../sx'
 import classes from './TextArea.module.css'
+import type {WithSlotMarker} from '../utils/types'
 
 export const DEFAULT_TEXTAREA_ROWS = 7
 export const DEFAULT_TEXTAREA_COLS = 30
@@ -106,5 +107,6 @@ const Textarea = React.forwardRef<HTMLTextAreaElement, TextareaProps>(
 )
 
 Textarea.displayName = 'Textarea'
+;(Textarea as WithSlotMarker<typeof Textarea>).__SLOT__ = Symbol('Textarea')
 
-export default Textarea
+export default Textarea as WithSlotMarker<typeof Textarea>
diff --git a/packages/react/src/Tooltip/Tooltip.tsx b/packages/react/src/Tooltip/Tooltip.tsx
index 2dec29b89d8..8122db14ae5 100644
--- a/packages/react/src/Tooltip/Tooltip.tsx
+++ b/packages/react/src/Tooltip/Tooltip.tsx
@@ -56,4 +56,6 @@ Tooltip.alignments = ['left', 'right']
 
 Tooltip.directions = ['n', 'ne', 'e', 'se', 's', 'sw', 'w', 'nw']
 
+Tooltip.__SLOT__ = Symbol('DEPRECATED_Tooltip')
+
 export default Tooltip
diff --git a/packages/react/src/TooltipV2/Tooltip.tsx b/packages/react/src/TooltipV2/Tooltip.tsx
index a291ecc9e10..cd4411a0dd9 100644
--- a/packages/react/src/TooltipV2/Tooltip.tsx
+++ b/packages/react/src/TooltipV2/Tooltip.tsx
@@ -1,4 +1,4 @@
-import React, {Children, useEffect, useRef, useState, useMemo} from 'react'
+import React, {Children, useEffect, useRef, useState, useMemo, type ForwardRefExoticComponent} from 'react'
 import {useId, useProvidedRefOrCreate, useOnEscapePress, useIsMacOS} from '../hooks'
 import {invariant} from '../utils/invariant'
 import {warning} from '../utils/warning'
@@ -10,6 +10,7 @@ import classes from './Tooltip.module.css'
 import {getAccessibleKeybindingHintString, KeybindingHint, type KeybindingHintProps} from '../KeybindingHint'
 import VisuallyHidden from '../_VisuallyHidden'
 import useSafeTimeout from '../hooks/useSafeTimeout'
+import type {SlotMarker} from '../utils/types'
 
 export type TooltipDirection = 'nw' | 'n' | 'ne' | 'e' | 'se' | 's' | 'sw' | 'w'
 export type TooltipProps = React.PropsWithChildren<{
@@ -92,7 +93,10 @@ const isInteractive = (element: HTMLElement) => {
 }
 export const TooltipContext = React.createContext<{tooltipId?: string}>({})
 
-export const Tooltip = React.forwardRef(
+export const Tooltip: ForwardRefExoticComponent<
+  React.PropsWithoutRef<TooltipProps> & React.RefAttributes<HTMLElement>
+> &
+  SlotMarker = React.forwardRef<HTMLElement, TooltipProps>(
   (
     {
       direction = 's',
@@ -361,3 +365,5 @@ export const Tooltip = React.forwardRef(
     )
   },
 )
+
+Tooltip.__SLOT__ = Symbol('Tooltip')
diff --git a/packages/react/src/__tests__/__snapshots__/exports.test.ts.snap b/packages/react/src/__tests__/__snapshots__/exports.test.ts.snap
index 4057c681ce2..dcb72ad996b 100644
--- a/packages/react/src/__tests__/__snapshots__/exports.test.ts.snap
+++ b/packages/react/src/__tests__/__snapshots__/exports.test.ts.snap
@@ -152,6 +152,7 @@ exports[`@primer/react > should not update exports without a semver change 1`] =
   "type SideNavProps",
   "SkeletonBox",
   "type SkeletonBoxProps",
+  "type SlotMarker",
   "Spinner",
   "type SpinnerProps",
   "SplitPageLayout",
diff --git a/packages/react/src/experimental/SelectPanel2/SelectPanel.tsx b/packages/react/src/experimental/SelectPanel2/SelectPanel.tsx
index 099d0dc5f24..5d97938d2be 100644
--- a/packages/react/src/experimental/SelectPanel2/SelectPanel.tsx
+++ b/packages/react/src/experimental/SelectPanel2/SelectPanel.tsx
@@ -27,6 +27,7 @@ import {clsx} from 'clsx'
 
 import classes from './SelectPanel.module.css'
 import type {PositionSettings} from '@primer/behaviors'
+import type {FCWithSlotMarker} from '../../utils/types'
 
 const SelectPanelContext = React.createContext<{
   title: string
@@ -340,7 +341,7 @@ const SelectPanelButton = React.forwardRef<HTMLButtonElement, ButtonProps>((prop
   }
 })
 
-const SelectPanelHeader: React.FC<React.ComponentPropsWithoutRef<'div'> & {onBack?: () => void}> = ({
+const SelectPanelHeader: FCWithSlotMarker<React.ComponentPropsWithoutRef<'div'> & {onBack?: () => void}> = ({
   children,
   onBack,
   className,
@@ -409,7 +410,9 @@ const SelectPanelHeader: React.FC<React.ComponentPropsWithoutRef<'div'> & {onBac
   )
 }
 
-const SelectPanelSearchInput: React.FC<TextInputProps> = ({
+SelectPanelHeader.__SLOT__ = Symbol('SelectPanel.Header')
+
+const SelectPanelSearchInput: FCWithSlotMarker<TextInputProps> = ({
   onChange: propsOnChange,
   onKeyDown: propsOnKeyDown,
   className,
@@ -465,6 +468,8 @@ const SelectPanelSearchInput: React.FC<TextInputProps> = ({
   )
 }
 
+SelectPanelSearchInput.__SLOT__ = Symbol('SelectPanel.SearchInput')
+
 const FooterContext = React.createContext<boolean>(false)
 const SelectPanelFooter = ({...props}) => {
   const {onCancel, selectionVariant} = React.useContext(SelectPanelContext)
@@ -500,6 +505,8 @@ const SelectPanelFooter = ({...props}) => {
   )
 }
 
+SelectPanelFooter.__SLOT__ = Symbol('SelectPanel.Footer')
+
 const SecondaryButton: React.FC<ButtonProps> = props => {
   const size = useResponsiveValue(responsiveButtonSizes, 'small')
   return <Button type="button" size={size} block {...props} />
diff --git a/packages/react/src/experimental/UnderlinePanels/UnderlinePanels.tsx b/packages/react/src/experimental/UnderlinePanels/UnderlinePanels.tsx
index ece7047c3e4..7dd02c34482 100644
--- a/packages/react/src/experimental/UnderlinePanels/UnderlinePanels.tsx
+++ b/packages/react/src/experimental/UnderlinePanels/UnderlinePanels.tsx
@@ -24,6 +24,8 @@ import {useResizeObserver, type ResizeObserverEntry} from '../../hooks/useResize
 import useIsomorphicLayoutEffect from '../../utils/useIsomorphicLayoutEffect'
 import classes from './UnderlinePanels.module.css'
 import {clsx} from 'clsx'
+import {isSlot} from '../../utils/is-slot'
+import type {FCWithSlotMarker} from '../../utils/types'
 
 export type UnderlinePanelsProps = {
   /**
@@ -75,7 +77,7 @@ export type PanelProps = React.HTMLAttributes<HTMLDivElement>
 
 const TabContainerComponent = createComponent(TabContainerElement, 'tab-container')
 
-const UnderlinePanels: FC<UnderlinePanelsProps> = ({
+const UnderlinePanels: FCWithSlotMarker<UnderlinePanelsProps> = ({
   'aria-label': ariaLabel,
   'aria-labelledby': ariaLabelledBy,
   children,
@@ -101,11 +103,11 @@ const UnderlinePanels: FC<UnderlinePanelsProps> = ({
     let panelIndex = 0
 
     const childrenWithProps = Children.map(children, child => {
-      if (isValidElement<UnderlineItemProps<ElementType>>(child) && child.type === Tab) {
+      if (isValidElement<UnderlineItemProps<ElementType>>(child) && (child.type === Tab || isSlot(child, Tab))) {
         return cloneElement(child, {id: `${parentId}-tab-${tabIndex++}`, loadingCounters, iconsVisible})
       }
 
-      if (isValidElement<PanelProps>(child) && child.type === Panel) {
+      if (isValidElement<PanelProps>(child) && (child.type === Panel || isSlot(child, Panel))) {
         const childPanel = child as React.ReactElement<PanelProps>
         return cloneElement(childPanel, {'aria-labelledby': `${parentId}-tab-${panelIndex++}`})
       }
@@ -113,11 +115,11 @@ const UnderlinePanels: FC<UnderlinePanelsProps> = ({
     })
 
     const newTabs = Children.toArray(childrenWithProps).filter(child => {
-      return isValidElement(child) && child.type === Tab
+      return isValidElement(child) && (child.type === Tab || isSlot(child, Tab))
     })
 
     const newTabPanels = Children.toArray(childrenWithProps).filter(
-      child => isValidElement(child) && child.type === Panel,
+      child => isValidElement(child) && (child.type === Panel || isSlot(child, Panel)),
     )
 
     setTabs(newTabs)
@@ -185,7 +187,7 @@ const UnderlinePanels: FC<UnderlinePanelsProps> = ({
   )
 }
 
-const Tab: FC<TabProps> = ({'aria-selected': ariaSelected, onSelect, ...props}) => {
+const Tab: FCWithSlotMarker<TabProps> = ({'aria-selected': ariaSelected, onSelect, ...props}) => {
   const clickHandler = React.useCallback(
     (event: React.MouseEvent<HTMLButtonElement, MouseEvent>) => {
       if (!event.defaultPrevented && typeof onSelect === 'function') {
@@ -219,7 +221,7 @@ const Tab: FC<TabProps> = ({'aria-selected': ariaSelected, onSelect, ...props})
 
 Tab.displayName = 'UnderlinePanels.Tab'
 
-const Panel: FC<PanelProps> = ({children, ...rest}) => {
+const Panel: FCWithSlotMarker<PanelProps> = ({children, ...rest}) => {
   return (
     <div role="tabpanel" {...rest}>
       {children}
@@ -230,3 +232,7 @@ const Panel: FC<PanelProps> = ({children, ...rest}) => {
 Panel.displayName = 'UnderlinePanels.Panel'
 
 export default Object.assign(UnderlinePanels, {Panel, Tab})
+
+UnderlinePanels.__SLOT__ = Symbol('UnderlinePanels')
+Tab.__SLOT__ = Symbol('UnderlinePanels.Tab')
+Panel.__SLOT__ = Symbol('UnderlinePanels.Panel')
diff --git a/packages/react/src/hooks/__tests__/useSlots.test.tsx b/packages/react/src/hooks/__tests__/useSlots.test.tsx
index 3a25be6ba5e..b342fa5ddc5 100644
--- a/packages/react/src/hooks/__tests__/useSlots.test.tsx
+++ b/packages/react/src/hooks/__tests__/useSlots.test.tsx
@@ -9,10 +9,50 @@ function TestComponentA(props: TestComponentAProps) {
   return <div {...props} />
 }
 
+TestComponentA.__SLOT__ = Symbol('TestComponentA')
+
 function TestComponentB(props: React.PropsWithChildren<unknown>) {
   return <div {...props} />
 }
 
+// Test components with slot symbols
+function TestComponentWithSlot(props: React.PropsWithChildren<unknown>) {
+  return <div {...props} />
+}
+
+TestComponentWithSlot.__SLOT__ = Symbol('TestComponentWithSlot')
+
+function TestComponentWithSlotVariant(props: TestComponentAProps) {
+  return <div {...props} />
+}
+
+TestComponentWithSlotVariant.__SLOT__ = Symbol('TestComponentWithSlotVariant')
+
+// Wrapper components that use the slot symbol from the original component
+const WrappedTestComponentA = () => (
+  <div>
+    <TestComponentA>Wrapped A</TestComponentA>
+  </div>
+)
+
+WrappedTestComponentA.__SLOT__ = TestComponentA.__SLOT__
+
+const WrappedTestComponentWithSlot = () => (
+  <div>
+    <TestComponentWithSlot>Wrapped with slot</TestComponentWithSlot>
+  </div>
+)
+
+WrappedTestComponentWithSlot.__SLOT__ = TestComponentWithSlot.__SLOT__
+
+const WrappedTestComponentWithSlotVariant = (props: TestComponentAProps) => (
+  <div>
+    <TestComponentWithSlotVariant {...props}>Wrapped variant</TestComponentWithSlotVariant>
+  </div>
+)
+
+WrappedTestComponentWithSlotVariant.__SLOT__ = TestComponentWithSlotVariant.__SLOT__
+
 test('extracts elements based on config object', () => {
   const calls: Array<ReturnType<typeof useSlots>> = []
   const children = [<TestComponentA key="a" />, <TestComponentB key="b" />, <div key="hello">Hello World</div>]
@@ -207,3 +247,287 @@ test('extracts elements based on condition in config object', () => {
     ]
   `)
 })
+
+test('extracts components using slot symbols', () => {
+  const calls: Array<ReturnType<typeof useSlots>> = []
+  const children = [
+    <TestComponentWithSlot key="slot">Slot content</TestComponentWithSlot>,
+    <TestComponentB key="b">Regular B</TestComponentB>,
+    <div key="hello">Hello World</div>,
+  ]
+  const slotsConfig = {
+    slotComponent: TestComponentWithSlot,
+    b: TestComponentB,
+  }
+
+  function TestComponent(_props: {children: React.ReactNode}) {
+    calls.push(useSlots(children, slotsConfig))
+    return null
+  }
+
+  render(<TestComponent>{children}</TestComponent>)
+
+  expect(calls).toMatchInlineSnapshot(`
+    [
+      [
+        {
+          "b": <TestComponentB>
+            Regular B
+          </TestComponentB>,
+          "slotComponent": <TestComponentWithSlot>
+            Slot content
+          </TestComponentWithSlot>,
+        },
+        [
+          <div>
+            Hello World
+          </div>,
+        ],
+      ],
+    ]
+  `)
+})
+
+test('extracts wrapped components using slot symbols', () => {
+  const calls: Array<ReturnType<typeof useSlots>> = []
+  const children = [
+    <WrappedTestComponentWithSlot key="wrapped" />,
+    <TestComponentB key="b">Regular B</TestComponentB>,
+    <div key="hello">Hello World</div>,
+  ]
+  const slotsConfig = {
+    slotComponent: TestComponentWithSlot,
+    b: TestComponentB,
+  }
+
+  function TestComponent(_props: {children: React.ReactNode}) {
+    calls.push(useSlots(children, slotsConfig))
+    return null
+  }
+
+  render(<TestComponent>{children}</TestComponent>)
+
+  expect(calls).toMatchInlineSnapshot(`
+    [
+      [
+        {
+          "b": <TestComponentB>
+            Regular B
+          </TestComponentB>,
+          "slotComponent": <WrappedTestComponentWithSlot />,
+        },
+        [
+          <div>
+            Hello World
+          </div>,
+        ],
+      ],
+    ]
+  `)
+})
+
+test('extracts wrapped components with slot symbols and conditions', () => {
+  const calls: Array<ReturnType<typeof useSlots>> = []
+  const children = [
+    <WrappedTestComponentWithSlotVariant key="variant-a" variant="a" />,
+    <WrappedTestComponentWithSlotVariant key="variant-b" variant="b" />,
+    <div key="hello">Hello World</div>,
+  ]
+
+  function TestComponent(_props: {children: React.ReactNode}) {
+    calls.push(
+      useSlots(children, {
+        variantA: [TestComponentWithSlotVariant, (props: TestComponentAProps) => props.variant === 'a'],
+        variantB: [TestComponentWithSlotVariant, (props: TestComponentAProps) => props.variant === 'b'],
+      }),
+    )
+    return null
+  }
+
+  render(<TestComponent>{children}</TestComponent>)
+
+  expect(calls).toMatchInlineSnapshot(`
+    [
+      [
+        {
+          "variantA": <WrappedTestComponentWithSlotVariant
+            variant="a"
+          />,
+          "variantB": <WrappedTestComponentWithSlotVariant
+            variant="b"
+          />,
+        },
+        [
+          <div>
+            Hello World
+          </div>,
+        ],
+      ],
+    ]
+  `)
+})
+
+test('prefers direct component type match over slot symbol match', () => {
+  const calls: Array<ReturnType<typeof useSlots>> = []
+  const children = [
+    <TestComponentWithSlot key="direct">Direct component</TestComponentWithSlot>,
+    <WrappedTestComponentWithSlot key="wrapped" />,
+    <div key="hello">Hello World</div>,
+  ]
+  const slotsConfig = {
+    slotComponent: TestComponentWithSlot,
+  }
+
+  function TestComponent(_props: {children: React.ReactNode}) {
+    calls.push(useSlots(children, slotsConfig))
+    return null
+  }
+
+  render(<TestComponent>{children}</TestComponent>)
+
+  expect(calls).toMatchInlineSnapshot(`
+    [
+      [
+        {
+          "slotComponent": <TestComponentWithSlot>
+            Direct component
+          </TestComponentWithSlot>,
+        },
+        [
+          <div>
+            Hello World
+          </div>,
+        ],
+      ],
+    ]
+  `)
+})
+
+test('handles components without slot symbols in mixed scenarios', () => {
+  const calls: Array<ReturnType<typeof useSlots>> = []
+  const children = [
+    <TestComponentA key="a">Component A</TestComponentA>,
+    <WrappedTestComponentA key="wrapped" />,
+    <TestComponentWithSlot key="slot">Slot component</TestComponentWithSlot>,
+    <div key="hello">Hello World</div>,
+  ]
+  const slotsConfig = {
+    a: TestComponentA,
+    slotComponent: TestComponentWithSlot,
+  }
+
+  function TestComponent(_props: {children: React.ReactNode}) {
+    calls.push(useSlots(children, slotsConfig))
+    return null
+  }
+
+  render(<TestComponent>{children}</TestComponent>)
+
+  expect(calls).toMatchInlineSnapshot(`
+    [
+      [
+        {
+          "a": <TestComponentA>
+            Component A
+          </TestComponentA>,
+          "slotComponent": <TestComponentWithSlot>
+            Slot component
+          </TestComponentWithSlot>,
+        },
+        [
+          <div>
+            Hello World
+          </div>,
+        ],
+      ],
+    ]
+  `)
+})
+
+test('handles slot symbol matching with duplicate detection', () => {
+  const calls: Array<ReturnType<typeof useSlots>> = []
+  const warnSpy = vi.spyOn(console, 'warn').mockImplementation(() => {})
+  const children = [
+    <TestComponentWithSlot key="first">First slot</TestComponentWithSlot>,
+    <WrappedTestComponentWithSlot key="wrapped" />,
+    <div key="hello">Hello World</div>,
+  ]
+  const slotsConfig = {
+    slotComponent: TestComponentWithSlot,
+  }
+
+  function TestComponent(_props: {children: React.ReactNode}) {
+    calls.push(useSlots(children, slotsConfig))
+    return null
+  }
+
+  render(<TestComponent>{children}</TestComponent>)
+
+  expect(calls).toMatchInlineSnapshot(`
+    [
+      [
+        {
+          "slotComponent": <TestComponentWithSlot>
+            First slot
+          </TestComponentWithSlot>,
+        },
+        [
+          <div>
+            Hello World
+          </div>,
+        ],
+      ],
+    ]
+  `)
+  expect(warnSpy).toHaveBeenCalledTimes(1)
+  expect(warnSpy).toHaveBeenCalledWith(
+    'Warning:',
+    'Found duplicate "slotComponent" slot. Only the first will be rendered.',
+  )
+})
+
+test('handles empty slot symbols gracefully', () => {
+  const calls: Array<ReturnType<typeof useSlots>> = []
+
+  // Component without __SLOT__ property
+  function ComponentWithoutSlot(props: React.PropsWithChildren<unknown>) {
+    return <div {...props} />
+  }
+
+  const children = [
+    <ComponentWithoutSlot key="no-slot">No slot</ComponentWithoutSlot>,
+    <TestComponentWithSlot key="with-slot">With slot</TestComponentWithSlot>,
+    <div key="hello">Hello World</div>,
+  ]
+  const slotsConfig = {
+    slotComponent: TestComponentWithSlot,
+    noSlot: ComponentWithoutSlot,
+  }
+
+  function TestComponent(_props: {children: React.ReactNode}) {
+    calls.push(useSlots(children, slotsConfig))
+    return null
+  }
+
+  render(<TestComponent>{children}</TestComponent>)
+
+  expect(calls).toMatchInlineSnapshot(`
+    [
+      [
+        {
+          "noSlot": <ComponentWithoutSlot>
+            No slot
+          </ComponentWithoutSlot>,
+          "slotComponent": <TestComponentWithSlot>
+            With slot
+          </TestComponentWithSlot>,
+        },
+        [
+          <div>
+            Hello World
+          </div>,
+        ],
+      ],
+    ]
+  `)
+})
diff --git a/packages/react/src/hooks/useSlots.ts b/packages/react/src/hooks/useSlots.ts
index 9fb3d824b29..965c512c83e 100644
--- a/packages/react/src/hooks/useSlots.ts
+++ b/packages/react/src/hooks/useSlots.ts
@@ -1,5 +1,7 @@
 import React from 'react'
 import {warning} from '../utils/warning'
+import {isSlot} from '../utils/is-slot'
+import type {SlotMarker} from '../utils/types'
 
 // slot config allows 2 options:
 // 1. Component to match, example: { leadingVisual: LeadingVisual }
@@ -55,9 +57,9 @@ export function useSlots<Config extends SlotConfig>(
     const index = values.findIndex(value => {
       if (Array.isArray(value)) {
         const [component, testFn] = value
-        return child.type === component && testFn(child.props)
+        return (child.type === component || isSlot(child, component as SlotMarker)) && testFn(child.props)
       } else {
-        return child.type === value
+        return child.type === value || isSlot(child, value as SlotMarker)
       }
     })
 
diff --git a/packages/react/src/index.ts b/packages/react/src/index.ts
index f4fc3fa7669..56f9268070c 100644
--- a/packages/react/src/index.ts
+++ b/packages/react/src/index.ts
@@ -51,6 +51,7 @@ export {useSyncedState} from './hooks/useSyncedState'
 
 // Utils
 export {createComponent} from './utils/create-component'
+export type {SlotMarker} from './utils/types'
 
 // Components
 export {default as Radio} from './Radio'
diff --git a/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupCaption.tsx b/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupCaption.tsx
index 7b89c12fc0a..a77f2a9f474 100644
--- a/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupCaption.tsx
+++ b/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupCaption.tsx
@@ -3,10 +3,11 @@ import Text from '../../../Text'
 import CheckboxOrRadioGroupContext from './CheckboxOrRadioGroupContext'
 import classes from './CheckboxOrRadioGroup.module.css'
 import {clsx} from 'clsx'
+import type {FCWithSlotMarker} from '../../../utils/types'
 
 type CheckboxOrRadioGroupCaptionProps = React.PropsWithChildren<{className?: string}>
 
-const CheckboxOrRadioGroupCaption: React.FC<CheckboxOrRadioGroupCaptionProps> = ({className, children}) => {
+const CheckboxOrRadioGroupCaption: FCWithSlotMarker<CheckboxOrRadioGroupCaptionProps> = ({className, children}) => {
   const {captionId} = React.useContext(CheckboxOrRadioGroupContext)
   return (
     <Text className={clsx(className, classes.CheckboxOrRadioGroupCaption)} id={captionId}>
@@ -16,3 +17,5 @@ const CheckboxOrRadioGroupCaption: React.FC<CheckboxOrRadioGroupCaptionProps> =
 }
 
 export default CheckboxOrRadioGroupCaption
+
+CheckboxOrRadioGroupCaption.__SLOT__ = Symbol('CheckboxGroup.Caption')
diff --git a/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupLabel.tsx b/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupLabel.tsx
index 8970f1ef61c..2f6058ea8b9 100644
--- a/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupLabel.tsx
+++ b/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupLabel.tsx
@@ -4,6 +4,7 @@ import CheckboxOrRadioGroupContext from './CheckboxOrRadioGroupContext'
 import classes from './CheckboxOrRadioGroup.module.css'
 import {Stack} from '../../../Stack'
 import {clsx} from 'clsx'
+import type {FCWithSlotMarker} from '../../../utils/types'
 
 export type CheckboxOrRadioGroupLabelProps = {
   /** Class name for custom styling */
@@ -14,7 +15,7 @@ export type CheckboxOrRadioGroupLabelProps = {
   visuallyHidden?: boolean
 }
 
-const CheckboxOrRadioGroupLabel: React.FC<React.PropsWithChildren<CheckboxOrRadioGroupLabelProps>> = ({
+const CheckboxOrRadioGroupLabel: FCWithSlotMarker<React.PropsWithChildren<CheckboxOrRadioGroupLabelProps>> = ({
   children,
   className,
   visuallyHidden = false,
@@ -41,3 +42,5 @@ const CheckboxOrRadioGroupLabel: React.FC<React.PropsWithChildren<CheckboxOrRadi
 }
 
 export default CheckboxOrRadioGroupLabel
+
+CheckboxOrRadioGroupLabel.__SLOT__ = Symbol('CheckboxGroup.Label')
diff --git a/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupValidation.tsx b/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupValidation.tsx
index c42928622be..13988fa66f8 100644
--- a/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupValidation.tsx
+++ b/packages/react/src/internal/components/CheckboxOrRadioGroup/CheckboxOrRadioGroupValidation.tsx
@@ -2,16 +2,16 @@ import React from 'react'
 import InputValidation from '../InputValidation'
 import type {FormValidationStatus} from '../../../utils/types/FormValidationStatus'
 import CheckboxOrRadioGroupContext from './CheckboxOrRadioGroupContext'
+import type {FCWithSlotMarker} from '../../../utils/types'
 
 export type CheckboxOrRadioGroupValidationProps = {
   /** Changes the visual style to match the validation status */
   variant: FormValidationStatus
 }
 
-const CheckboxOrRadioGroupValidation: React.FC<React.PropsWithChildren<CheckboxOrRadioGroupValidationProps>> = ({
-  children,
-  variant,
-}) => {
+const CheckboxOrRadioGroupValidation: FCWithSlotMarker<
+  React.PropsWithChildren<CheckboxOrRadioGroupValidationProps>
+> = ({children, variant}) => {
   const {validationMessageId = ''} = React.useContext(CheckboxOrRadioGroupContext)
   return (
     <InputValidation validationStatus={variant} id={validationMessageId}>
@@ -21,3 +21,5 @@ const CheckboxOrRadioGroupValidation: React.FC<React.PropsWithChildren<CheckboxO
 }
 
 export default CheckboxOrRadioGroupValidation
+
+CheckboxOrRadioGroupValidation.__SLOT__ = Symbol('CheckboxGroup.Validation')
diff --git a/packages/react/src/utils/is-slot.ts b/packages/react/src/utils/is-slot.ts
new file mode 100644
index 00000000000..d39dc0704f7
--- /dev/null
+++ b/packages/react/src/utils/is-slot.ts
@@ -0,0 +1,16 @@
+import type {SlotMarker, WithSlotMarker} from './types'
+
+/**
+ * Determines whether a given element is a valid slot for the supplied slot component
+ */
+export function isSlot(element: unknown, slot: WithSlotMarker<unknown>): boolean {
+  const elementType = typeof element
+
+  if (elementType !== 'object' && elementType !== 'function' && element != null) {
+    return false
+  }
+  const reactElement = element as {type?: SlotMarker} & SlotMarker
+
+  const elementSlot = reactElement.__SLOT__ ?? reactElement.type?.__SLOT__
+  return slot.__SLOT__ ? elementSlot === slot.__SLOT__ : false
+}
diff --git a/packages/react/src/utils/polymorphic.ts b/packages/react/src/utils/polymorphic.ts
index 04e61883c55..cf697986bb6 100644
--- a/packages/react/src/utils/polymorphic.ts
+++ b/packages/react/src/utils/polymorphic.ts
@@ -6,6 +6,7 @@
  */
 
 import * as React from 'react'
+import type {SlotMarker} from './types/Slots'
 
 /* -------------------------------------------------------------------------------------------------
  * Utility types
@@ -37,7 +38,8 @@ interface ForwardRefComponent<
    * Extends original type to ensure built in React types play nice
    * with polymorphic components still e.g. `React.ElementRef` etc.
    */
-> extends ForwardRefExoticComponent<IntrinsicElementString, OwnProps> {
+> extends ForwardRefExoticComponent<IntrinsicElementString, OwnProps>,
+    SlotMarker {
   /**
    * When `as` prop is passed, use this overload.
    * Merges original own props (without DOM props) and the inferred props
diff --git a/packages/react/src/utils/types/Slots.ts b/packages/react/src/utils/types/Slots.ts
new file mode 100644
index 00000000000..5d6cc57eea4
--- /dev/null
+++ b/packages/react/src/utils/types/Slots.ts
@@ -0,0 +1,8 @@
+export interface SlotMarker {
+  /** Marker to denote the custom child slot for a component */
+  __SLOT__?: symbol
+}
+
+export type WithSlotMarker<T> = T & SlotMarker
+
+export type FCWithSlotMarker<P> = WithSlotMarker<React.FC<P>>
diff --git a/packages/react/src/utils/types/index.ts b/packages/react/src/utils/types/index.ts
index 315f090d8a6..a5446438eb1 100644
--- a/packages/react/src/utils/types/index.ts
+++ b/packages/react/src/utils/types/index.ts
@@ -3,3 +3,4 @@ export * from './ComponentProps'
 export * from './Flatten'
 export * from './Merge'
 export * from './MandateProps'
+export * from './Slots'
diff --git a/packages/styled-react/src/__tests__/primer-react.browser.test.tsx b/packages/styled-react/src/__tests__/primer-react.browser.test.tsx
index ef35220fe97..6d1370ffe9b 100644
--- a/packages/styled-react/src/__tests__/primer-react.browser.test.tsx
+++ b/packages/styled-react/src/__tests__/primer-react.browser.test.tsx
@@ -389,9 +389,11 @@ describe('@primer/react', () => {
 
   test('SegmentedControl.Button supports `sx` prop', () => {
     render(
-      <SegmentedControl.Button data-testid="component" sx={{background: 'red'}}>
-        test
-      </SegmentedControl.Button>,
+      <SegmentedControl>
+        <SegmentedControl.Button data-testid="component" sx={{background: 'red'}}>
+          test
+        </SegmentedControl.Button>
+      </SegmentedControl>,
     )
     const buttonElement = screen.getByTestId('component')
     expect(window.getComputedStyle(buttonElement).backgroundColor).toBe('rgb(255, 0, 0)')
diff --git a/packages/styled-react/src/components/ActionList.tsx b/packages/styled-react/src/components/ActionList.tsx
index 1d5f3e5a375..454517eb7e0 100644
--- a/packages/styled-react/src/components/ActionList.tsx
+++ b/packages/styled-react/src/components/ActionList.tsx
@@ -9,6 +9,7 @@ import {
   type ActionListDividerProps as PrimerActionListDividerProps,
   type ActionListLeadingVisualProps as PrimerActionListLeadingVisualProps,
   type ActionListTrailingVisualProps as PrimerActionListTrailingVisualProps,
+  type SlotMarker,
 } from '@primer/react'
 import {sx, type SxProp} from '../sx'
 import type {ForwardRefComponent} from '../polymorphic'
@@ -39,7 +40,7 @@ const ActionListImpl = React.forwardRef(function ActionListImpl<As extends React
   return <StyledActionList ref={ref} {...rest} {...(as ? {forwardedAs: as} : {})} />
 })
 
-const ActionListLinkItem: ForwardRefComponent<'a', ActionListLinkItemProps> = styled(
+const ActionListLinkItem: ForwardRefComponent<'a', ActionListLinkItemProps> & SlotMarker = styled(
   PrimerActionList.LinkItem,
 ).withConfig<ActionListLinkItemProps>({
   shouldForwardProp: prop => prop !== 'sx',
@@ -65,7 +66,7 @@ const ActionListTrailingAction = React.forwardRef<HTMLButtonElement | HTMLAnchor
       />
     )
   },
-) as ForwardRefComponent<TrailingActionElements, ActionListTrailingActionProps>
+) as ForwardRefComponent<TrailingActionElements, ActionListTrailingActionProps> & SlotMarker
 
 const StyledActionListItem: ForwardRefComponent<'li', ActionListItemProps> = styled(
   PrimerActionList.Item,
@@ -79,9 +80,9 @@ const ActionListItem = React.forwardRef<HTMLLIElement, ActionListItemProps>(({ch
   <StyledActionListItem ref={ref} {...props} {...(as ? {forwardedAs: as} : {})}>
     {children}
   </StyledActionListItem>
-)) as ForwardRefComponent<'li', ActionListItemProps>
+)) as ForwardRefComponent<'li', ActionListItemProps> & SlotMarker
 
-const ActionListGroup: React.ComponentType<ActionListGroupProps> = styled(
+const ActionListGroup: React.ComponentType<ActionListGroupProps> & SlotMarker = styled(
   PrimerActionList.Group,
 ).withConfig<ActionListGroupProps>({
   shouldForwardProp: prop => prop !== 'sx',
@@ -89,7 +90,7 @@ const ActionListGroup: React.ComponentType<ActionListGroupProps> = styled(
   ${sx}
 `
 
-const ActionListDivider: React.ComponentType<ActionListDividerProps> = styled(
+const ActionListDivider: React.ComponentType<ActionListDividerProps> & SlotMarker = styled(
   PrimerActionList.Divider,
 ).withConfig<ActionListDividerProps>({
   shouldForwardProp: prop => prop !== 'sx',
@@ -97,7 +98,7 @@ const ActionListDivider: React.ComponentType<ActionListDividerProps> = styled(
   ${sx}
 `
 
-const ActionListLeadingVisual: React.ComponentType<ActionListLeadingVisualProps> = styled(
+const ActionListLeadingVisual: React.ComponentType<ActionListLeadingVisualProps> & SlotMarker = styled(
   PrimerActionList.LeadingVisual,
 ).withConfig<ActionListLeadingVisualProps>({
   shouldForwardProp: prop => prop !== 'sx',
@@ -105,7 +106,7 @@ const ActionListLeadingVisual: React.ComponentType<ActionListLeadingVisualProps>
   ${sx}
 `
 
-const ActionListTrailingVisual: React.ComponentType<ActionListTrailingVisualProps> = styled(
+const ActionListTrailingVisual: React.ComponentType<ActionListTrailingVisualProps> & SlotMarker = styled(
   PrimerActionList.TrailingVisual,
 ).withConfig<ActionListTrailingVisualProps>({
   shouldForwardProp: prop => prop !== 'sx',
@@ -124,7 +125,7 @@ export const ActionList: typeof ActionListImpl & {
   TrailingVisual: typeof ActionListTrailingVisual
   Heading: typeof PrimerActionList.Heading
   TrailingAction: typeof ActionListTrailingAction
-} = Object.assign(ActionListImpl, {
+} & SlotMarker = Object.assign(ActionListImpl, {
   Item: ActionListItem,
   LinkItem: ActionListLinkItem,
   Group: ActionListGroup,
@@ -136,3 +137,12 @@ export const ActionList: typeof ActionListImpl & {
   Heading: PrimerActionList.Heading,
   TrailingAction: ActionListTrailingAction,
 })
+
+// Assign slot markers after component definitions
+ActionListItem.__SLOT__ = PrimerActionList.Item.__SLOT__
+ActionListLinkItem.__SLOT__ = PrimerActionList.LinkItem.__SLOT__
+ActionListGroup.__SLOT__ = PrimerActionList.Group.__SLOT__
+ActionListDivider.__SLOT__ = PrimerActionList.Divider.__SLOT__
+ActionListLeadingVisual.__SLOT__ = PrimerActionList.LeadingVisual.__SLOT__
+ActionListTrailingVisual.__SLOT__ = PrimerActionList.TrailingVisual.__SLOT__
+ActionListTrailingAction.__SLOT__ = PrimerActionList.TrailingAction.__SLOT__
diff --git a/packages/styled-react/src/components/ActionMenu.tsx b/packages/styled-react/src/components/ActionMenu.tsx
index dbb89ecf7b2..61759b78173 100644
--- a/packages/styled-react/src/components/ActionMenu.tsx
+++ b/packages/styled-react/src/components/ActionMenu.tsx
@@ -1,11 +1,13 @@
-import {ActionMenu as PrimerActionMenu, type SxProp} from '@primer/react'
+import {ActionMenu as PrimerActionMenu, type SxProp, type SlotMarker} from '@primer/react'
 import {sx} from '../sx'
 import styled from 'styled-components'
 import type {ComponentProps} from 'react'
 
 type ActionMenuOverlayProps = ComponentProps<typeof PrimerActionMenu.Overlay> & SxProp
 
-const ActionMenuOverlay: React.ComponentType<ActionMenuOverlayProps> = styled(PrimerActionMenu.Overlay).withConfig({
+const ActionMenuOverlay: React.ComponentType<ActionMenuOverlayProps> & SlotMarker = styled(
+  PrimerActionMenu.Overlay,
+).withConfig({
   shouldForwardProp: prop => (prop as keyof ActionMenuOverlayProps) !== 'sx',
 })`
   ${sx}
@@ -22,3 +24,5 @@ export const ActionMenu: typeof PrimerActionMenu & {
   Overlay: ActionMenuOverlay,
   Divider: PrimerActionMenu.Divider,
 })
+
+ActionMenuOverlay.__SLOT__ = PrimerActionMenu.Overlay.__SLOT__
diff --git a/packages/styled-react/src/components/Autocomplete.tsx b/packages/styled-react/src/components/Autocomplete.tsx
index 2028c65d111..1ee6e899f35 100644
--- a/packages/styled-react/src/components/Autocomplete.tsx
+++ b/packages/styled-react/src/components/Autocomplete.tsx
@@ -1,6 +1,7 @@
 import {
   Autocomplete as PrimerAutocomplete,
   type AutocompleteOverlayProps as PrimerAutocompleteOverlayProps,
+  type SlotMarker,
 } from '@primer/react'
 import {sx, type SxProp} from '../sx'
 import styled from 'styled-components'
@@ -8,7 +9,7 @@ import type {ComponentProps} from 'react'
 
 export type AutocompleteOverlayProps = PrimerAutocompleteOverlayProps & SxProp
 
-const AutocompleteOverlay: React.ComponentType<AutocompleteOverlayProps> = styled(
+const AutocompleteOverlay: React.ComponentType<AutocompleteOverlayProps> & SlotMarker = styled(
   PrimerAutocomplete.Overlay,
 ).withConfig({
   shouldForwardProp: prop => (prop as keyof AutocompleteOverlayProps) !== 'sx',
@@ -31,4 +32,6 @@ const Autocomplete: AutocompleteExport = Object.assign(PrimerAutocomplete, {
   Overlay: AutocompleteOverlay,
 })
 
+AutocompleteOverlay.__SLOT__ = PrimerAutocomplete.Overlay.__SLOT__
+
 export {Autocomplete}
diff --git a/packages/styled-react/src/components/Checkbox.tsx b/packages/styled-react/src/components/Checkbox.tsx
index f8ee4411c81..3cdd244603b 100644
--- a/packages/styled-react/src/components/Checkbox.tsx
+++ b/packages/styled-react/src/components/Checkbox.tsx
@@ -1,4 +1,4 @@
-import {Checkbox as PrimerCheckbox, type CheckboxProps as PrimerCheckboxProps} from '@primer/react'
+import {Checkbox as PrimerCheckbox, type CheckboxProps as PrimerCheckboxProps, type SlotMarker} from '@primer/react'
 import {Box} from './Box'
 import {forwardRef} from 'react'
 import {type SxProp} from '../sx'
@@ -8,3 +8,4 @@ export type CheckboxProps = PrimerCheckboxProps & SxProp
 export const Checkbox = forwardRef<HTMLInputElement, CheckboxProps>(function Checkbox(props, ref) {
   return <Box as={PrimerCheckbox} ref={ref} {...props} />
 })
+;(Checkbox as typeof Checkbox & SlotMarker).__SLOT__ = PrimerCheckbox.__SLOT__
diff --git a/packages/styled-react/src/components/CheckboxGroup.tsx b/packages/styled-react/src/components/CheckboxGroup.tsx
index 7af793f8403..cdb5468daab 100644
--- a/packages/styled-react/src/components/CheckboxGroup.tsx
+++ b/packages/styled-react/src/components/CheckboxGroup.tsx
@@ -47,3 +47,8 @@ export const CheckboxGroup = Object.assign(CheckboxGroupImpl, {
   Caption: CheckboxOrRadioGroupCaption,
   Validation: CheckboxOrRadioGroupValidation,
 })
+
+CheckboxGroupImpl.__SLOT__ = PrimerCheckboxGroup.__SLOT__
+CheckboxOrRadioGroupLabel.__SLOT__ = PrimerCheckboxGroup.Label.__SLOT__
+CheckboxOrRadioGroupCaption.__SLOT__ = PrimerCheckboxGroup.Caption.__SLOT__
+CheckboxOrRadioGroupValidation.__SLOT__ = PrimerCheckboxGroup.Validation.__SLOT__
diff --git a/packages/styled-react/src/components/PageLayout.tsx b/packages/styled-react/src/components/PageLayout.tsx
index 882c18c3504..2d296ca8620 100644
--- a/packages/styled-react/src/components/PageLayout.tsx
+++ b/packages/styled-react/src/components/PageLayout.tsx
@@ -4,6 +4,7 @@ import type {
   PageLayoutProps as PrimerPageLayoutProps,
   PageLayoutContentProps as PrimerPageLayoutContentProps,
   PageLayoutPaneProps as PrimerPageLayoutPaneProps,
+  SlotMarker,
 } from '@primer/react'
 import {PageLayout as PrimerPageLayout} from '@primer/react'
 import {sx, type SxProp} from '../sx'
@@ -31,11 +32,22 @@ const PageLayoutPane = React.forwardRef<HTMLDivElement, PageLayoutPaneProps>((pr
   return <Wrapper as={PrimerPageLayout.Pane} ref={ref} {...props} />
 })
 
-const PageLayout = Object.assign(PageLayoutImpl, {
+type PageLayoutType = typeof PageLayoutImpl & {
+  Content: typeof PageLayoutContent
+  Header: typeof PrimerPageLayout.Header
+  Pane: typeof PageLayoutPane
+  Footer: typeof PrimerPageLayout.Footer
+}
+
+const PageLayout: PageLayoutType = Object.assign(PageLayoutImpl, {
+  __SLOT__: PrimerPageLayout.__SLOT__,
   Content: PageLayoutContent,
   Header: PrimerPageLayout.Header,
   Pane: PageLayoutPane,
   Footer: PrimerPageLayout.Footer,
 })
 
+;(PageLayoutContent as typeof PageLayoutContent & SlotMarker).__SLOT__ = PrimerPageLayout.Content.__SLOT__
+;(PageLayoutPane as typeof PageLayoutPane & SlotMarker).__SLOT__ = PrimerPageLayout.Pane.__SLOT__
+
 export {PageLayout, type PageLayoutProps}
diff --git a/packages/styled-react/src/components/RadioGroup.tsx b/packages/styled-react/src/components/RadioGroup.tsx
index 2e5a9ba5af7..4a8ab2ecec2 100644
--- a/packages/styled-react/src/components/RadioGroup.tsx
+++ b/packages/styled-react/src/components/RadioGroup.tsx
@@ -43,3 +43,8 @@ export const RadioGroup = Object.assign(RadioGroupImpl, {
   Caption: CheckboxOrRadioGroupCaption,
   Validation: CheckboxOrRadioGroupValidation,
 })
+
+RadioGroupImpl.__SLOT__ = PrimerRadioGroup.__SLOT__
+CheckboxOrRadioGroupLabel.__SLOT__ = PrimerRadioGroup.Label.__SLOT__
+CheckboxOrRadioGroupCaption.__SLOT__ = PrimerRadioGroup.Caption.__SLOT__
+CheckboxOrRadioGroupValidation.__SLOT__ = PrimerRadioGroup.Validation.__SLOT__
diff --git a/packages/styled-react/src/components/SegmentedControl.tsx b/packages/styled-react/src/components/SegmentedControl.tsx
index 86ea27bed35..cc6a50efe52 100644
--- a/packages/styled-react/src/components/SegmentedControl.tsx
+++ b/packages/styled-react/src/components/SegmentedControl.tsx
@@ -25,10 +25,14 @@ const SegmentedControlImpl = (props: SegmentedControlProps) => {
 }
 
 const SegmentedControl = Object.assign(SegmentedControlImpl, {
+  __SLOT__: PrimerSegmentedControl.__SLOT__,
   Button: SegmentedControlButton,
   IconButton: SegmentedControlIconButton,
 })
 
+SegmentedControlButton.__SLOT__ = PrimerSegmentedControl.Button.__SLOT__
+SegmentedControlIconButton.__SLOT__ = PrimerSegmentedControl.IconButton.__SLOT__
+
 export {
   SegmentedControl,
   type SegmentedControlProps,
diff --git a/packages/styled-react/src/components/SubNav.tsx b/packages/styled-react/src/components/SubNav.tsx
index fb61f2038c7..b5d07b599e8 100644
--- a/packages/styled-react/src/components/SubNav.tsx
+++ b/packages/styled-react/src/components/SubNav.tsx
@@ -2,6 +2,7 @@ import {
   SubNav as PrimerSubNav,
   type SubNavProps as PrimerSubNavProps,
   type SubNavLinkProps as PrimerSubNavLinkProps,
+  type SlotMarker,
 } from '@primer/react'
 import {forwardRef} from 'react'
 import {Box} from './Box'
@@ -20,7 +21,10 @@ const SubNavLink = forwardRef<HTMLAnchorElement, SubNavLinkProps>(function SubNa
 })
 
 const SubNav = Object.assign(SubNavImpl, {
+  __SLOT__: PrimerSubNav.__SLOT__,
   Link: SubNavLink,
 })
 
+;(SubNavLink as typeof SubNavLink & SlotMarker).__SLOT__ = PrimerSubNav.Link.__SLOT__
+
 export {SubNav, type SubNavProps, type SubNavLinkProps}
diff --git a/packages/styled-react/src/components/Tooltip.tsx b/packages/styled-react/src/components/Tooltip.tsx
index ba3bbfb34d8..001c8d5008d 100644
--- a/packages/styled-react/src/components/Tooltip.tsx
+++ b/packages/styled-react/src/components/Tooltip.tsx
@@ -1,14 +1,21 @@
-import {Tooltip as PrimerTooltip, type TooltipProps as PrimerTooltipProps, type SxProp} from '@primer/react'
+import {
+  Tooltip as PrimerTooltip,
+  type TooltipProps as PrimerTooltipProps,
+  type SxProp,
+  type SlotMarker,
+} from '@primer/react'
 import {Box} from './Box'
 import {forwardRef, type ForwardRefExoticComponent, type RefAttributes} from 'react'
 
 type TooltipProps = PrimerTooltipProps & SxProp
 
-const Tooltip: ForwardRefExoticComponent<TooltipProps & RefAttributes<HTMLDivElement>> = forwardRef<
+const Tooltip: ForwardRefExoticComponent<TooltipProps & RefAttributes<HTMLDivElement>> & SlotMarker = forwardRef<
   HTMLDivElement,
   TooltipProps
 >(function Tooltip(props, ref) {
   return <Box as={PrimerTooltip} ref={ref} {...props} />
 })
 
+Tooltip.__SLOT__ = PrimerTooltip.__SLOT__
+
 export {Tooltip, type TooltipProps}
diff --git a/packages/styled-react/src/components/UnderlinePanels.tsx b/packages/styled-react/src/components/UnderlinePanels.tsx
index d310ed39d39..18ae4676051 100644
--- a/packages/styled-react/src/components/UnderlinePanels.tsx
+++ b/packages/styled-react/src/components/UnderlinePanels.tsx
@@ -22,9 +22,14 @@ const UnderlinePanelsImpl = ({as, ...props}: UnderlinePanelsProps) => (
 
 UnderlinePanelsImpl.displayName = 'UnderlinePanels'
 
-const UnderlinePanels = Object.assign(UnderlinePanelsImpl, {
+const UnderlinePanels: typeof UnderlinePanelsImpl & {
+  Tab: typeof PrimerUnderlinePanels.Tab
+  Panel: typeof PrimerUnderlinePanels.Panel
+} = Object.assign(UnderlinePanelsImpl, {
   Tab: PrimerUnderlinePanels.Tab,
   Panel: PrimerUnderlinePanels.Panel,
 })
 
+UnderlinePanelsImpl.__SLOT__ = PrimerUnderlinePanels.__SLOT__
+
 export {UnderlinePanels, type UnderlinePanelsProps, type UnderlinePanelsTabProps, type UnderlinePanelsPanelProps}
diff --git a/packages/styled-react/src/components/deprecated/Tooltip.tsx b/packages/styled-react/src/components/deprecated/Tooltip.tsx
index 9af0200ffb9..c3fc4cf76a3 100644
--- a/packages/styled-react/src/components/deprecated/Tooltip.tsx
+++ b/packages/styled-react/src/components/deprecated/Tooltip.tsx
@@ -3,6 +3,7 @@ import {forwardRef} from 'react'
 import {sx, type SxProp} from '../../sx'
 import {type PropsWithChildren} from 'react'
 import styled from 'styled-components'
+import type {SlotMarker} from '@primer/react'
 
 // Add explicit `as` prop since polymorphic typing doesn't carry over to type aliases
 type TooltipProps = PropsWithChildren<PrimerTooltipProps & SxProp & {as?: React.ElementType}>
@@ -25,5 +26,6 @@ const Tooltip = TooltipImpl as typeof TooltipImpl & {
 // Preserve static properties from the original component
 Tooltip.alignments = PrimerTooltip.alignments
 Tooltip.directions = PrimerTooltip.directions
+;(Tooltip as typeof Tooltip & SlotMarker).__SLOT__ = PrimerTooltip.__SLOT__
 
 export {Tooltip, type TooltipProps}