diff --git a/src/core/project/manager.test.ts b/src/core/project/manager.test.ts
index a355dc4b4..5ba5d1b71 100644
--- a/src/core/project/manager.test.ts
+++ b/src/core/project/manager.test.ts
@@ -330,4 +330,29 @@ describe("FsProjectManager.resolve", () => {
       InputValidationError,
     );
   });
+
+  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(
+      "runtimes[0].runtimeVersion: runtimeVersion is required for CodeZip builds",
+    );
+  });
 });
diff --git a/src/core/project/manager.tsx b/src/core/project/manager.tsx
index c23f4d960..9a9de2999 100644
--- a/src/core/project/manager.tsx
+++ b/src/core/project/manager.tsx
@@ -20,6 +20,29 @@ import { createProjectTreeFromTemplate, TEMPLATES } from "./templates";
 import { ProjectSpecSchema } from "../../projectSchemas/project";
 import { enclosingProjectRoot } from "./fsUtils";
 import { DeserializationError, InputValidationError, ProjectStateError } from "../../errors/errors";
+import { z } from "zod";
+
+/**
+ * Renders the reasons a spec failed validation, as `runtimes[0].runtimeVersion: <why>`.
+ * Without this the cause is only reachable from the debug log, leaving the user with
+ * "invalid project configuration" and no indication of which field to fix.
+ */
+function describeValidationFailure(cause: unknown): string {
+  if (!(cause instanceof z.ZodError)) return "";
+  return cause.issues
+    .map((issue) => {
+      const field = issue.path.reduce<string>(
+        (rendered, segment) =>
+          typeof segment === "number" ? `${rendered}[${segment}]` : appendKey(rendered, segment),
+        "",
+      );
+      return `\n  - ${field === "" ? "(root)" : field}: ${issue.message}`;
+    })
+    .join("");
+}
+
+const appendKey = (rendered: string, segment: PropertyKey): string =>
+  rendered === "" ? String(segment) : `${rendered}.${String(segment)}`;
 
 type ProjectManagerConfig = {
   logger: Logger;
@@ -63,9 +86,10 @@ export class FsProjectManager implements ProjectManager {
     } 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 new InputValidationError(
+          `invalid project configuration at ${configPath}${describeValidationFailure(error.cause)}`,
+          { cause: error },
+        );
       }
       throw error;
     }
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({