diff --git a/agent/error_classifier.py b/agent/error_classifier.py
index 9d830cdc996..33c2f545856 100644
--- a/agent/error_classifier.py
+++ b/agent/error_classifier.py
@@ -413,6 +413,7 @@ _CONTENT_POLICY_BLOCKED_PATTERNS = [
 _AUTH_PATTERNS = [
     "invalid api key",
     "invalid_api_key",
+    "gateway_auth_failed",
     "authentication",
     "unauthorized",
     "forbidden",
diff --git a/apps/desktop/src/store/notifications.ts b/apps/desktop/src/store/notifications.ts
index 92f41163506..97bfc31d541 100644
--- a/apps/desktop/src/store/notifications.ts
+++ b/apps/desktop/src/store/notifications.ts
@@ -78,7 +78,11 @@ function cleanErrorText(value: string) {
 
 const ERROR_SUMMARIES: { test: (msg: string) => boolean; summarize: (msg: string) => string }[] = [
   {
-    test: msg => /incorrect api key provided/i.test(msg) || /['"]code['"]\s*:\s*['"]invalid_api_key['"]/i.test(msg),
+    test: msg => /['"']code['"']\s*:\s*['"']gateway_auth_failed['"']/i.test(msg),
+    summarize: () => 'Gateway authentication failed — check your API_SERVER_KEY.'
+  },
+  {
+    test: msg => /incorrect api key provided/i.test(msg) || /['"']code['"']\s*:\s*['"']invalid_api_key['"']/i.test(msg),
     summarize: msg => {
       const status = msg.match(/(?:error code|status(?:Code)?)[^\d]*(\d{3})/i)?.[1]
 
diff --git a/gateway/platforms/api_server.py b/gateway/platforms/api_server.py
index f2af8566639..c888fef3d3b 100644
--- a/gateway/platforms/api_server.py
+++ b/gateway/platforms/api_server.py
@@ -1335,7 +1335,7 @@ class APIServerAdapter(BasePlatformAdapter):
             self._request_audit_log_suffix(request),
         )
         return web.json_response(
-            {"error": {"message": "Invalid API key", "type": "invalid_request_error", "code": "invalid_api_key"}},
+            {"error": {"message": "Invalid gateway API key (API_SERVER_KEY)", "type": "gateway_auth_error", "code": "gateway_auth_failed"}},
             status=401,
         )
 
diff --git a/tests/gateway/test_session_api.py b/tests/gateway/test_session_api.py
index 47f7b38eec4..ac6314f2d28 100644
--- a/tests/gateway/test_session_api.py
+++ b/tests/gateway/test_session_api.py
@@ -416,7 +416,7 @@ async def test_session_endpoints_require_auth_when_key_configured(auth_adapter):
         resp = await cli.get("/api/sessions")
         assert resp.status == 401
         body = await resp.json()
-        assert body["error"]["code"] == "invalid_api_key"
+        assert body["error"]["code"] == "gateway_auth_failed"
 
         ok = await cli.get("/api/sessions", headers={"Authorization": "Bearer sk-test"})
         assert ok.status == 200