diff --git a/end-to-end/organization_token_test.go b/end-to-end/organization_token_test.go
index fb5c86467..8572ee483 100644
--- a/end-to-end/organization_token_test.go
+++ b/end-to-end/organization_token_test.go
@@ -67,7 +67,7 @@ func TestOrganizationProvidedToken(t *testing.T) {
 				require.NoErrorf(t, err, "Setup: could not wake distro up: %v. %s", err, out)
 			}
 
-			const maxTimeout = 15 * time.Second
+			const maxTimeout = 30 * time.Second
 
 			if !tc.wantAttached {
 				time.Sleep(maxTimeout)
diff --git a/gui/packages/ubuntupro/lib/pages/startup/agent_monitor.dart b/gui/packages/ubuntupro/lib/pages/startup/agent_monitor.dart
index 9dee12778..962557e6f 100644
--- a/gui/packages/ubuntupro/lib/pages/startup/agent_monitor.dart
+++ b/gui/packages/ubuntupro/lib/pages/startup/agent_monitor.dart
@@ -79,7 +79,7 @@ class AgentStartupMonitor {
   /// The loop stops if a terminal condition is found or [timeout] expires.
   Stream<AgentState> start({
     Duration interval = const Duration(seconds: 1),
-    Duration timeout = const Duration(seconds: 30),
+    Duration timeout = const Duration(seconds: 5),
   }) async* {
     if (_addrFilePath == null) {
       // Terminal state, cannot recover nor retry.
@@ -127,10 +127,16 @@ class AgentStartupMonitor {
         // Terminal state, cannot recover nor retry.
         return AgentState.unknownEnv;
       case AgentAddrFileError.nonexistent:
+        // The directory must exist so we can watch for changes. This won't fail if the directory already exists.
+        final agentDir = await File(_addrFilePath!).parent.create();
+        final watch = agentDir
+            .watch(events: FileSystemEvent.create)
+            .firstWhere((event) => event.path.contains(_addrFilePath!));
         if (!await agentLauncher()) {
           // Terminal state, cannot recover nor retry.
           return AgentState.cannotStart;
         }
+        await watch;
         return AgentState.starting;
       // maybe a race condition allowed us to read the file before write completed? Retry.
       // ignore: switch_case_completes_normally
diff --git a/gui/packages/ubuntupro/test/startup/agent_monitor_test.dart b/gui/packages/ubuntupro/test/startup/agent_monitor_test.dart
index 6f8b4a5fd..68e2d1132 100644
--- a/gui/packages/ubuntupro/test/startup/agent_monitor_test.dart
+++ b/gui/packages/ubuntupro/test/startup/agent_monitor_test.dart
@@ -191,6 +191,32 @@ void main() {
     verify(mockClient.ping()).called(1);
   });
 
+  test('timeout if never addr', () async {
+    final mockClient = MockAgentApiClient();
+    // Fakes a successful ping.
+    when(mockClient.ping()).thenAnswer((_) async => true);
+    final monitor = AgentStartupMonitor(
+      /// A launch request will always succeed, but never writes the addr file.
+      agentLauncher: () async {
+        return true;
+      },
+      clientFactory: (port) => mockClient,
+      appName: kAppName,
+      addrFileName: kAddrFileName,
+      onClient: (_) {},
+    );
+
+    await expectLater(
+      monitor.start(interval: kInterval),
+      emitsInOrder([
+        AgentState.querying,
+        // instead of waiting the addr file to show up forever, we are caught by our internal timeout.
+        AgentState.unreachable,
+      ]),
+    );
+    verifyNever(mockClient.ping());
+  });
+
   test('await async onClient callback', () async {
     final completeMe = Completer<void>();
     final mockClient = MockAgentApiClient();
diff --git a/gui/packages/ubuntupro/test/startup/startup_model_test.mocks.dart b/gui/packages/ubuntupro/test/startup/startup_model_test.mocks.dart
index c7cd6a758..d0fc23031 100644
--- a/gui/packages/ubuntupro/test/startup/startup_model_test.mocks.dart
+++ b/gui/packages/ubuntupro/test/startup/startup_model_test.mocks.dart
@@ -61,7 +61,7 @@ class MockAgentStartupMonitor extends _i1.Mock
   @override
   _i4.Stream<_i3.AgentState> start({
     Duration? interval = const Duration(seconds: 1),
-    Duration? timeout = const Duration(seconds: 30),
+    Duration? timeout = const Duration(seconds: 5),
   }) =>
       (super.noSuchMethod(
         Invocation.method(
diff --git a/gui/packages/ubuntupro/test/startup/startup_page_test.mocks.dart b/gui/packages/ubuntupro/test/startup/startup_page_test.mocks.dart
index 07b451ece..fbf2e0226 100644
--- a/gui/packages/ubuntupro/test/startup/startup_page_test.mocks.dart
+++ b/gui/packages/ubuntupro/test/startup/startup_page_test.mocks.dart
@@ -73,7 +73,7 @@ class MockAgentStartupMonitor extends _i1.Mock
   @override
   _i5.Stream<_i4.AgentState> start({
     Duration? interval = const Duration(seconds: 1),
-    Duration? timeout = const Duration(seconds: 30),
+    Duration? timeout = const Duration(seconds: 5),
   }) =>
       (super.noSuchMethod(
         Invocation.method(