diff --git a/src/core/dev/container.test.ts b/src/core/dev/container.test.ts
index 3767c88aa..c8ece4891 100644
--- a/src/core/dev/container.test.ts
+++ b/src/core/dev/container.test.ts
@@ -11,7 +11,7 @@ import {
   type ProcessStreamer,
   type StreamProcessOptions,
 } from "../../io";
-import type { ProjectRuntime } from "../project/schema";
+import type { ProjectRuntime } from "../../projectSchemas/runtime";
 import { ContainerDevRunner } from "./container";
 
 type ProcessCall = {
diff --git a/src/core/project/manager.test.ts b/src/core/project/manager.test.ts
index a355dc4b4..27085ea2c 100644
--- a/src/core/project/manager.test.ts
+++ b/src/core/project/manager.test.ts
@@ -2,7 +2,7 @@ import { afterEach, describe, expect, test } from "bun:test";
 import { mkdir, mkdtemp, readdir, rm, writeFile } from "node:fs/promises";
 import { join, relative } from "node:path";
 import { tmpdir } from "node:os";
-import { InputValidationError, ProjectStateError } from "../../errors/errors";
+import { DeserializationError, ProjectStateError } from "../../errors/errors";
 import { FsProjectManager } from "./manager";
 import {
   PROJECT_TEMPLATES,
@@ -327,7 +327,32 @@ describe("FsProjectManager.resolve", () => {
     await writeFile(join(root, "agentcore", "agentcore.json"), "{ not valid json");
 
     await expect(manager().manager.resolve({ filePath: root })).rejects.toBeInstanceOf(
-      InputValidationError,
+      DeserializationError,
+    );
+  });
+
+  test("names the offending field when the spec fails validation", async () => {
+    const root = await inTempDirectory();
+    await mkdir(join(root, "agentcore"), { recursive: true });
+    // Valid JSON, invalid spec: a CodeZip runtime with no runtimeVersion.
+    await writeFile(
+      join(root, "agentcore", "agentcore.json"),
+      JSON.stringify({
+        name: "example",
+        version: 1,
+        runtimes: [
+          {
+            name: "hello_world",
+            build: "CodeZip",
+            entrypoint: "main.py",
+            codeLocation: "app/hello-world",
+          },
+        ],
+      }),
+    );
+
+    await expect(manager().manager.resolve({ filePath: root })).rejects.toThrow(
+      "runtimeVersion is required for CodeZip builds",
     );
   });
 });
diff --git a/src/core/project/manager.tsx b/src/core/project/manager.tsx
index c23f4d960..0859d34c3 100644
--- a/src/core/project/manager.tsx
+++ b/src/core/project/manager.tsx
@@ -19,7 +19,7 @@ import { defaultSource, type AssetSource } from "./source";
 import { createProjectTreeFromTemplate, TEMPLATES } from "./templates";
 import { ProjectSpecSchema } from "../../projectSchemas/project";
 import { enclosingProjectRoot } from "./fsUtils";
-import { DeserializationError, InputValidationError, ProjectStateError } from "../../errors/errors";
+import { ProjectStateError } from "../../errors/errors";
 
 type ProjectManagerConfig = {
   logger: Logger;
@@ -52,23 +52,13 @@ export class FsProjectManager implements ProjectManager {
     if (!rootPath) return undefined;
 
     const configPath = join(rootPath, "agentcore", "agentcore.json");
-    try {
-      const spec = await this.json.read(configPath, ProjectSpecSchema);
-      return {
-        name: spec.name,
-        rootPath,
-        managedBy: spec.managedBy,
-        runtimes: spec.runtimes,
-      };
-    } catch (error) {
-      // A malformed agentcore.json is a user-correctable problem, not a crash.
-      if (error instanceof DeserializationError) {
-        throw new InputValidationError(`invalid project configuration at ${configPath}`, {
-          cause: error,
-        });
-      }
-      throw error;
-    }
+    const spec = await this.json.read(configPath, ProjectSpecSchema);
+    return {
+      name: spec.name,
+      rootPath,
+      managedBy: spec.managedBy,
+      runtimes: spec.runtimes,
+    };
   }
 
   public async *create(input: CreateProjectInput): AsyncGenerator<ProjectEvent, Project> {
diff --git a/src/errors/errors.tsx b/src/errors/errors.tsx
index 262ac8d4d..7fae0222a 100644
--- a/src/errors/errors.tsx
+++ b/src/errors/errors.tsx
@@ -90,11 +90,13 @@ export class SourceResolutionError extends InputValidationError {
   }
 }
 
-// TODO: attach telemetry metadata to this error class.
-export class DeserializationError extends Error {
-  constructor(path: string, options?: { cause?: unknown }) {
-    super(`Failed to deserialize JSON at "${path}"`, options);
-    this.name = "DeserializationError";
+export class DeserializationError extends AgentCoreCLIError {
+  constructor(path: string, options?: { cause?: unknown; detail?: string }) {
+    const detail = options?.detail ? `\n${options.detail}` : "";
+    super(`Failed to deserialize JSON at "${path}"${detail}`, {
+      ...options,
+      source: ERROR_SOURCE.USER,
+    });
   }
 }
 
diff --git a/src/io/json.ts b/src/io/json.ts
index 082f72b71..064b1481c 100644
--- a/src/io/json.ts
+++ b/src/io/json.ts
@@ -2,6 +2,7 @@ import { mkdir, readFile, writeFile } from "node:fs/promises";
 import { dirname } from "node:path";
 
 import type z from "zod";
+import { prettifyError } from "zod";
 
 import { DeserializationError } from "../errors";
 import type { Logger } from "../logging";
@@ -52,7 +53,10 @@ export class FsReadWriteJson implements ReadWriteJson {
           errorMessage: parseResult.error.message,
         })
         .error(`failed to validate parsed json file`);
-      throw new DeserializationError(filePath, { cause: parseResult.error });
+      throw new DeserializationError(filePath, {
+        cause: parseResult.error,
+        detail: prettifyError(parseResult.error),
+      });
     }
 
     return parseResult.data;
diff --git a/src/projectSchemas/project.test.ts b/src/projectSchemas/project.test.ts
index 123e9a0c9..8a9b89842 100644
--- a/src/projectSchemas/project.test.ts
+++ b/src/projectSchemas/project.test.ts
@@ -8,6 +8,7 @@ const runtime = {
   build: "CodeZip" as const,
   entrypoint: "main.py",
   codeLocation: "./agent",
+  runtimeVersion: "PYTHON_3_12" as const,
   endpoints: { LIVE: { version: 1 } },
 };
 
diff --git a/src/projectSchemas/runtime.test.ts b/src/projectSchemas/runtime.test.ts
index 5af245552..d752c2f4d 100644
--- a/src/projectSchemas/runtime.test.ts
+++ b/src/projectSchemas/runtime.test.ts
@@ -11,6 +11,7 @@ const codeZipAgent = {
   build: "CodeZip" as const,
   entrypoint: "main.py",
   codeLocation: "./agent",
+  runtimeVersion: "PYTHON_3_12" as const,
 };
 const containerAgent = {
   name: "agent",
@@ -72,6 +73,15 @@ describe("runtime custom validation", () => {
       }).success,
     ).toBe(false);
   });
+  it("requires runtimeVersion for CodeZip builds only", () => {
+    const { runtimeVersion: _omitted, ...withoutVersion } = codeZipAgent;
+    const result = ProjectRuntimeSchema.safeParse(withoutVersion);
+    expect(result.success).toBe(false);
+    expect(result.error?.issues[0]?.path).toEqual(["runtimeVersion"]);
+
+    // Container builds take their version from the image.
+    expect(ProjectRuntimeSchema.safeParse(containerAgent).success).toBe(true);
+  });
   it("restricts container-only fields to container builds", () => {
     for (const field of [
       { dockerfile: "Dockerfile" },
diff --git a/src/projectSchemas/runtime.ts b/src/projectSchemas/runtime.ts
index 61dc95886..f168ab480 100644
--- a/src/projectSchemas/runtime.ts
+++ b/src/projectSchemas/runtime.ts
@@ -308,6 +308,17 @@ export const ProjectRuntimeSchema = z
         path: ["authorizerConfiguration"],
       });
     }
+    // Mirrors the CDK construct library, which rejects a CodeZip runtime with no
+    // runtimeVersion: it is the field that selects the packager. Validating it here
+    // means the CLI reports it against agentcore.json instead of letting synthesis
+    // fail later with the same rule.
+    if (data.build !== "Container" && !data.runtimeVersion) {
+      ctx.addIssue({
+        code: "custom",
+        message: "runtimeVersion is required for CodeZip builds",
+        path: ["runtimeVersion"],
+      });
+    }
     for (const field of ["dockerfile", "buildContextPath", "customDockerBuildArgs"] as const) {
       if (data.build !== "Container" && data[field]) {
         ctx.addIssue({