diff --git a/server/src/__tests__/error-handler.test.ts b/server/src/__tests__/error-handler.test.ts
index 3d58f4fa27..cfd65a23a2 100644
--- a/server/src/__tests__/error-handler.test.ts
+++ b/server/src/__tests__/error-handler.test.ts
@@ -87,6 +87,31 @@ describe("errorHandler", () => {
     expect(res.__errorContext?.error?.message).toBe("db exploded");
   });
 
+  it("returns 400 for Zod validation errors from another module instance", () => {
+    const req = makeReq();
+    const res = makeRes() as any;
+    const next = vi.fn() as unknown as NextFunction;
+    const issue = {
+      code: "invalid_type",
+      expected: "string",
+      received: "undefined",
+      path: ["provider"],
+      message: "Required",
+    };
+    const err = Object.assign(new Error("Validation failed"), {
+      name: "ZodError",
+      issues: [issue],
+      errors: [issue],
+    });
+
+    errorHandler(err, req, res, next);
+
+    expect(res.status).toHaveBeenCalledWith(400);
+    expect(res.json).toHaveBeenCalledWith({ error: "Validation error", details: [issue] });
+    expect(res.err).toBeUndefined();
+    expect(res.__errorContext).toBeUndefined();
+  });
+
   it("records responsible-user denial codes on the active agent run", () => {
     const db = { marker: "db" };
     const req = {
diff --git a/server/src/middleware/error-handler.ts b/server/src/middleware/error-handler.ts
index 8937dfdcbc..5ba9ad5821 100644
--- a/server/src/middleware/error-handler.ts
+++ b/server/src/middleware/error-handler.ts
@@ -23,6 +23,13 @@ function isRedactedSkillPolicyDenial(details: Record<string, unknown> | null) {
   return details?.code === "skill_policy_denied";
 }
 
+function readZodIssues(err: unknown): unknown[] | null {
+  if (err instanceof ZodError) return err.issues;
+  if (!err || typeof err !== "object" || (err as { name?: unknown }).name !== "ZodError") return null;
+  const issues = (err as { issues?: unknown }).issues;
+  return Array.isArray(issues) ? issues : null;
+}
+
 function attachErrorContext(
   req: Request,
   res: Response,
@@ -117,8 +124,9 @@ export function errorHandler(
     return;
   }
 
-  if (err instanceof ZodError) {
-    res.status(400).json({ error: "Validation error", details: err.errors });
+  const zodIssues = readZodIssues(err);
+  if (zodIssues) {
+    res.status(400).json({ error: "Validation error", details: zodIssues });
     return;
   }