diff --git a/src/core/HttpResponse.ts b/src/core/HttpResponse.ts
index de3f6ea9d..ce13c747b 100644
--- a/src/core/HttpResponse.ts
+++ b/src/core/HttpResponse.ts
@@ -9,7 +9,7 @@ export interface HttpResponseInit extends ResponseInit {
   type?: ResponseType
 }
 
-declare const bodyType: unique symbol
+export declare const bodyType: unique symbol
 
 export interface StrictRequest<BodyType extends DefaultBodyType>
   extends Request {
diff --git a/src/core/handlers/RequestHandler.ts b/src/core/handlers/RequestHandler.ts
index 5c0c3ffa7..a09deb2e9 100644
--- a/src/core/handlers/RequestHandler.ts
+++ b/src/core/handlers/RequestHandler.ts
@@ -3,7 +3,7 @@ import { getCallFrame } from '../utils/internal/getCallFrame'
 import { isIterable } from '../utils/internal/isIterable'
 import type { ResponseResolutionContext } from '../utils/executeHandlers'
 import type { MaybePromise } from '../typeUtils'
-import { StrictRequest, StrictResponse } from '..//HttpResponse'
+import { StrictRequest, StrictResponse, bodyType } from '..//HttpResponse'
 
 export type DefaultRequestMultipartBody = Record<
   string,
@@ -38,14 +38,20 @@ export interface RequestHandlerInternalInfo {
 export type ResponseResolverReturnType<
   ResponseBodyType extends DefaultBodyType = undefined,
 > =
+  // If ResponseBodyType is a union, and one of the types is `undefined`,
+  // allow plain Response as the type.
   | ([ResponseBodyType] extends [undefined]
-      ? Response
-      : StrictResponse<ResponseBodyType>)
+      ? Response & { [bodyType]?: undefined }
+      : // If ResponseBodyType is exactly `undefined`,
+        // accept only the plain Response type.
+        ResponseBodyType extends undefined
+        ? Response & { [bodyType]?: undefined }
+        : StrictResponse<ResponseBodyType>)
   | undefined
   | void
 
 export type MaybeAsyncResponseResolverReturnType<
-  ResponseBodyType extends DefaultBodyType,
+  ResponseBodyType extends DefaultBodyType = undefined,
 > = MaybePromise<ResponseResolverReturnType<ResponseBodyType>>
 
 export type AsyncResponseResolverReturnType<
diff --git a/test/typings/graphql.test-d.ts b/test/typings/graphql.test-d.ts
index a4bdf2414..744f306f6 100644
--- a/test/typings/graphql.test-d.ts
+++ b/test/typings/graphql.test-d.ts
@@ -141,6 +141,12 @@ it('graphql handlers allow passthrough responses', () => {
   })
 })
 
+it('graphql handlers allow error response', () => {
+  graphql.query('GetUser', () => HttpResponse.error())
+  graphql.mutation('UpdatePost', () => HttpResponse.error())
+  graphql.operation(() => HttpResponse.error())
+})
+
 it("graphql variables cannot extract type from the runtime 'DocumentNode'", () => {
   /**
    * Supports `DocumentNode` as the GraphQL operation name.