diff --git a/changelog.d/fixes/12888-a2a-dashboard-auth.md b/changelog.d/fixes/12888-a2a-dashboard-auth.md
new file mode 100644
index 0000000000..8e6b45fa81
--- /dev/null
+++ b/changelog.d/fixes/12888-a2a-dashboard-auth.md
@@ -0,0 +1 @@
+- fix(a2a): accept the dashboard's own session cookie on /a2a so "Run message/send" no longer fails with "Unauthorized: missing or invalid API key" (#12888)
diff --git a/src/app/(dashboard)/dashboard/endpoint/components/A2ADashboard.tsx b/src/app/(dashboard)/dashboard/endpoint/components/A2ADashboard.tsx
index cc3bd7d072..278844cfd0 100644
--- a/src/app/(dashboard)/dashboard/endpoint/components/A2ADashboard.tsx
+++ b/src/app/(dashboard)/dashboard/endpoint/components/A2ADashboard.tsx
@@ -201,6 +201,7 @@ export default function A2ADashboardPage() {
       const response = await fetch("/a2a", {
         method: "POST",
         headers: { "Content-Type": "application/json" },
+        credentials: "same-origin",
         body: JSON.stringify({
           jsonrpc: "2.0",
           id: "dashboard-send",
@@ -234,6 +235,7 @@ export default function A2ADashboardPage() {
       const response = await fetch("/a2a", {
         method: "POST",
         headers: { "Content-Type": "application/json" },
+        credentials: "same-origin",
         body: JSON.stringify({
           jsonrpc: "2.0",
           id: "dashboard-stream",
diff --git a/src/app/a2a/route.ts b/src/app/a2a/route.ts
index dfe3fc73a7..4f023b53ff 100644
--- a/src/app/a2a/route.ts
+++ b/src/app/a2a/route.ts
@@ -187,7 +187,7 @@ export async function POST(req: NextRequest) {
   const tm = getTaskManager();
   // GHSA-jcm5-6wpp-wjj8: scope every task read/mutation below to the caller's
   // owner id (hashed API key; undefined under the keyless local-first posture).
-  const callerOwner = resolveA2AOwner(req);
+  const callerOwner = await resolveA2AOwner(req);
 
   // A2A 1.0 method-name compatibility (SendMessage → message/send, etc.)
   const isV1Method = method in V1_METHOD_ALIASES;
diff --git a/src/app/api/a2a/_auth.ts b/src/app/api/a2a/_auth.ts
index 2ec286db91..340fa20733 100644
--- a/src/app/api/a2a/_auth.ts
+++ b/src/app/api/a2a/_auth.ts
@@ -35,7 +35,7 @@ export async function authorizeA2ATaskRoute(request: Request): Promise<A2ARestAu
   const apiKey = extractApiKey(request);
 
   if (isRequireApiKeyEnabled()) {
-    if (apiKey && (await isValidApiKey(apiKey))) return { owner: resolveA2AOwner(request) };
+    if (apiKey && (await isValidApiKey(apiKey))) return { owner: await resolveA2AOwner(request) };
     const managementError = await requireManagementAuth(request, {
       invalidApiKeyStatus: 401,
       alwaysRequireAuth: true,
@@ -46,6 +46,6 @@ export async function authorizeA2ATaskRoute(request: Request): Promise<A2ARestAu
 
   const managementError = await requireManagementAuth(request, { invalidApiKeyStatus: 401 });
   if (managementError === null) return { owner: undefined };
-  if (apiKey && (await isValidApiKey(apiKey))) return { owner: resolveA2AOwner(request) };
+  if (apiKey && (await isValidApiKey(apiKey))) return { owner: await resolveA2AOwner(request) };
   return managementError;
 }
diff --git a/src/lib/a2a/authenticate.ts b/src/lib/a2a/authenticate.ts
index b57d4082cc..4d660d4d20 100644
--- a/src/lib/a2a/authenticate.ts
+++ b/src/lib/a2a/authenticate.ts
@@ -11,6 +11,7 @@
 import { createHash, timingSafeEqual } from "crypto";
 import type { NextRequest } from "next/server";
 import { extractApiKey, isValidApiKey } from "@/sse/services/auth";
+import { isDashboardSessionAuthenticated } from "@/shared/utils/apiAuth";
 import { isRequireApiKeyEnabled } from "@/shared/utils/featureFlags";
 
 function tokensMatch(provided: string, expected: string): boolean {
@@ -29,12 +30,17 @@ function tokensMatch(provided: string, expected: string): boolean {
 export async function authenticateA2ARequest(req: NextRequest | Request): Promise<boolean> {
   const apiKey = extractApiKey(req as NextRequest);
   if (isRequireApiKeyEnabled()) {
-    return apiKey ? await isValidApiKey(apiKey) : false;
+    if (apiKey) return isValidApiKey(apiKey);
+    // #12888: mirror clientApiPolicy's dashboard-session fallback so the
+    // dashboard's own A2A playground (no Authorization header, session
+    // cookie only) is accepted the same way /api/v1/* already accepts it.
+    return isDashboardSessionAuthenticated(req);
   }
 
   const configuredKey = process.env.OMNIROUTE_API_KEY;
   if (configuredKey) {
-    return apiKey ? tokensMatch(apiKey, configuredKey) : false;
+    if (apiKey) return tokensMatch(apiKey, configuredKey);
+    return isDashboardSessionAuthenticated(req);
   }
 
   // No API key required and none configured — allow (keyless local-first).
@@ -43,11 +49,15 @@ export async function authenticateA2ARequest(req: NextRequest | Request): Promis
 
 /**
  * Owner id for task scoping (GHSA-jcm5-6wpp-wjj8): a stable hash of the
- * caller's API key, or `undefined` when the call carries no key (keyless
- * posture — ownerless tasks stay visible to everyone, by design).
+ * caller's API key, `"dashboard"` for a session-authenticated caller with no
+ * API key (#12888 — keeps dashboard-originated tasks scoped consistently
+ * instead of falling into the ownerless keyless bucket), or `undefined` when
+ * the call carries neither (keyless posture — ownerless tasks stay visible to
+ * everyone, by design).
  */
-export function resolveA2AOwner(req: NextRequest | Request): string | undefined {
+export async function resolveA2AOwner(req: NextRequest | Request): Promise<string | undefined> {
   const apiKey = extractApiKey(req as NextRequest);
-  if (!apiKey) return undefined;
-  return createHash("sha256").update(apiKey).digest("hex").slice(0, 32);
+  if (apiKey) return createHash("sha256").update(apiKey).digest("hex").slice(0, 32);
+  if (await isDashboardSessionAuthenticated(req)) return "dashboard";
+  return undefined;
 }
diff --git a/tests/unit/a2a-dashboard-session-auth.test.ts b/tests/unit/a2a-dashboard-session-auth.test.ts
new file mode 100644
index 0000000000..79d20f3867
--- /dev/null
+++ b/tests/unit/a2a-dashboard-session-auth.test.ts
@@ -0,0 +1,57 @@
+import test from "node:test";
+import assert from "node:assert/strict";
+
+process.env.OMNIROUTE_API_KEY = "test-configured-key-12888";
+process.env.JWT_SECRET = "test-jwt-secret-for-probe-12888";
+
+const { authenticateA2ARequest, resolveA2AOwner } = await import("../../src/lib/a2a/authenticate.ts");
+const { isDashboardSessionAuthenticated } = await import("../../src/shared/utils/apiAuth.ts");
+const { SignJWT } = await import("jose");
+
+async function buildSessionRequest(): Promise<unknown> {
+  const secret = new TextEncoder().encode(process.env.JWT_SECRET);
+  const sessionToken = await new SignJWT({ authenticated: true })
+    .setProtectedHeader({ alg: "HS256" })
+    .setExpirationTime("30d")
+    .sign(secret);
+
+  return {
+    headers: new Headers({ cookie: `auth_token=${sessionToken}` }),
+    cookies: { get: () => undefined },
+    nextUrl: { searchParams: new URLSearchParams() },
+    url: "http://localhost:20128/a2a",
+  };
+}
+
+test("A2A route accepts a dashboard-session-authenticated request with no Authorization header (bug #12888)", async () => {
+  const fakeRequest = await buildSessionRequest();
+
+  const dashboardSessionOk = await isDashboardSessionAuthenticated(fakeRequest as never);
+  assert.equal(dashboardSessionOk, true, "expected the dashboard session cookie itself to be valid");
+
+  const a2aAuthOk = await authenticateA2ARequest(fakeRequest as never);
+  assert.equal(
+    a2aAuthOk,
+    true,
+    "/a2a should accept the dashboard's own session-authenticated requests " +
+      "(matching /api/v1/* behavior) but currently requires an explicit Authorization header"
+  );
+});
+
+test("A2A route still rejects a request with neither a valid API key nor a valid session cookie", async () => {
+  const fakeRequest = {
+    headers: new Headers(),
+    cookies: { get: () => undefined },
+    nextUrl: { searchParams: new URLSearchParams() },
+    url: "http://localhost:20128/a2a",
+  };
+
+  const a2aAuthOk = await authenticateA2ARequest(fakeRequest as never);
+  assert.equal(a2aAuthOk, false, "unauthenticated, keyless requests must still be rejected");
+});
+
+test("resolveA2AOwner() returns a stable 'dashboard' owner id for a session-authenticated caller with no API key", async () => {
+  const fakeRequest = await buildSessionRequest();
+  const owner = await resolveA2AOwner(fakeRequest as never);
+  assert.equal(owner, "dashboard");
+});
diff --git a/tests/unit/a2a-history-route.test.ts b/tests/unit/a2a-history-route.test.ts
index a4748bdf63..8ccdcced65 100644
--- a/tests/unit/a2a-history-route.test.ts
+++ b/tests/unit/a2a-history-route.test.ts
@@ -154,7 +154,7 @@ test("GET history owner-scoping: an API-key caller sees only its own + ownerless
   const ownerAReq = new Request("http://localhost/api/a2a/tasks/history", {
     headers: AUTH_HEADERS,
   });
-  const ownerA = resolveA2AOwner(ownerAReq as never);
+  const ownerA = await resolveA2AOwner(ownerAReq as never);
   assert.ok(ownerA, "the shared key resolves to a stable owner hash");
 
   seedRow({ id: "owned-by-a", apiKeyId: ownerA ?? null, createdAt: "2026-01-01T00:00:00.000Z" });
diff --git a/tests/unit/a2a-task-owner-idor.test.ts b/tests/unit/a2a-task-owner-idor.test.ts
index aaa35142c8..d05d4deffe 100644
--- a/tests/unit/a2a-task-owner-idor.test.ts
+++ b/tests/unit/a2a-task-owner-idor.test.ts
@@ -123,7 +123,7 @@ describe("REST /api/a2a/tasks/[id] — authentication (GHSA-jcm5)", () => {
     // And the same task IS visible to its owner (owner hash derived from the key).
     const owned = tm.createTask(
       { skill: "smart-routing", messages: [] },
-      resolveA2AOwner(req as never)
+      await resolveA2AOwner(req as never)
     );
     const res2 = await restGet.GET(
       new Request(`http://localhost/api/a2a/tasks/${owned.id}`, {