diff --git a/packages/flutter_driver/lib/src/driver/vmservice_driver.dart b/packages/flutter_driver/lib/src/driver/vmservice_driver.dart
index 9784c8f4f3..eff1bea7e0 100644
--- a/packages/flutter_driver/lib/src/driver/vmservice_driver.dart
+++ b/packages/flutter_driver/lib/src/driver/vmservice_driver.dart
@@ -127,27 +127,6 @@ class VMServiceFlutterDriver extends FlutterDriver {
 
     driver._dartVmReconnectUrl = dartVmServiceUrl;
 
-    // Attempts to resume the isolate, but does not crash if it fails because
-    // the isolate is already resumed. There could be a race with other tools,
-    // such as a debugger, any of which could have resumed the isolate.
-    Future<dynamic> resumeLeniently() {
-      _log('Attempting to resume isolate');
-      return isolate.resume().catchError((dynamic e) {
-        const int vmMustBePausedCode = 101;
-        if (e is rpc.RpcException && e.code == vmMustBePausedCode) {
-          // No biggie; something else must have resumed the isolate
-          _log(
-              'Attempted to resume an already resumed isolate. This may happen '
-                  'when we lose a race with another tool (usually a debugger) that '
-                  'is connected to the same isolate.'
-          );
-        } else {
-          // Failed to resume due to another reason. Fail hard.
-          throw e;
-        }
-      });
-    }
-
     /// Waits for a signal from the VM service that the extension is registered.
     ///
     /// Looks at the list of loaded extensions for the current [isolateRef], as
@@ -195,11 +174,18 @@ class VMServiceFlutterDriver extends FlutterDriver {
       });
     }
 
+    // The Dart VM may be running with --pause-isolates-on-start.
+    // Set a listener to unpause new isolates as they are ready to run,
+    // otherwise they'll hang indefinitely.
+    client.onIsolateRunnable.listen((VMIsolateRef isolateRef) async {
+      _resumeLeniently(await isolateRef.load());
+    });
+
     // Attempt to resume isolate if it was paused
     if (isolate.pauseEvent is VMPauseStartEvent) {
       _log('Isolate is paused at start.');
 
-      await resumeLeniently();
+      await _resumeLeniently(isolate);
     } else if (isolate.pauseEvent is VMPauseExitEvent ||
         isolate.pauseEvent is VMPauseBreakpointEvent ||
         isolate.pauseEvent is VMPauseExceptionEvent ||
@@ -207,7 +193,7 @@ class VMServiceFlutterDriver extends FlutterDriver {
       // If the isolate is paused for any other reason, assume the extension is
       // already there.
       _log('Isolate is paused mid-flight.');
-      await resumeLeniently();
+      await _resumeLeniently(isolate);
     } else if (isolate.pauseEvent is VMResumeEvent) {
       _log('Isolate is not paused. Assuming application is ready.');
     } else {
@@ -240,6 +226,27 @@ class VMServiceFlutterDriver extends FlutterDriver {
     return driver;
   }
 
+  /// Attempts to resume the isolate, but does not crash if it fails because
+  /// the isolate is already resumed. There could be a race with other tools,
+  /// such as a debugger, any of which could have resumed the isolate.
+  static Future<dynamic> _resumeLeniently(VMIsolate isolate) {
+    _log('Attempting to resume isolate');
+    return isolate.resume().catchError((dynamic e) {
+      const int vmMustBePausedCode = 101;
+      if (e is rpc.RpcException && e.code == vmMustBePausedCode) {
+        // No biggie; something else must have resumed the isolate
+        _log(
+            'Attempted to resume an already resumed isolate. This may happen '
+                'when we lose a race with another tool (usually a debugger) that '
+                'is connected to the same isolate.'
+        );
+      } else {
+        // Failed to resume due to another reason. Fail hard.
+        throw e;
+      }
+    });
+  }
+
   static int _nextDriverId = 0;
 
   static const String _flutterExtensionMethodName = 'ext.flutter.driver';
diff --git a/packages/flutter_driver/test/flutter_driver_test.dart b/packages/flutter_driver/test/flutter_driver_test.dart
index 5a2844d393..bcb0898dc5 100644
--- a/packages/flutter_driver/test/flutter_driver_test.dart
+++ b/packages/flutter_driver/test/flutter_driver_test.dart
@@ -35,6 +35,7 @@ void main() {
     MockVM mockVM;
     MockIsolate mockIsolate;
     MockPeer mockPeer;
+    MockIsolate otherIsolate;
 
     void expectLogContains(String message) {
       expect(log, anyElement(contains(message)));
@@ -45,8 +46,12 @@ void main() {
       mockClient = MockVMServiceClient();
       mockVM = MockVM();
       mockIsolate = MockIsolate();
+      otherIsolate = MockIsolate();
       mockPeer = MockPeer();
       when(mockClient.getVM()).thenAnswer((_) => Future<MockVM>.value(mockVM));
+      when(mockClient.onIsolateRunnable).thenAnswer((Invocation invocation) {
+        return Stream<VMIsolateRef>.fromIterable(<VMIsolateRef>[otherIsolate]);
+      });
       when(mockVM.isolates).thenReturn(<VMRunnableIsolate>[mockIsolate]);
       when(mockIsolate.loadRunnable()).thenAnswer((_) => Future<MockIsolate>.value(mockIsolate));
       when(mockIsolate.extensionRpcs).thenReturn(<String>[]);
@@ -60,6 +65,10 @@ void main() {
           VMServiceClientConnection(mockClient, mockPeer)
         );
       };
+      when(otherIsolate.load()).thenAnswer((_) => Future<MockIsolate>.value(otherIsolate));
+      when(otherIsolate.resume()).thenAnswer((Invocation invocation) {
+        return Future<dynamic>.value(null);
+      });
     });
 
     tearDown(() async {
@@ -77,15 +86,20 @@ void main() {
         connectionLog.add('resume');
         return Future<dynamic>.value(null);
       });
+      when(otherIsolate.pauseEvent).thenReturn(MockVMPauseStartEvent());
       when(mockIsolate.onExtensionAdded).thenAnswer((Invocation invocation) {
         connectionLog.add('onExtensionAdded');
         return Stream<String>.fromIterable(<String>['ext.flutter.driver']);
       });
+      when(otherIsolate.resume()).thenAnswer((Invocation invocation) {
+        connectionLog.add('other-resume');
+        return Future<dynamic>.value(null);
+      });
 
       final FlutterDriver driver = await FlutterDriver.connect(dartVmServiceUrl: '');
       expect(driver, isNotNull);
       expectLogContains('Isolate is paused at start');
-      expect(connectionLog, <String>['resume', 'streamListen', 'onExtensionAdded']);
+      expect(connectionLog, <String>['resume', 'streamListen', 'other-resume', 'onExtensionAdded']);
     });
 
     test('connects to isolate paused mid-flight', () async {