diff --git a/packages/flutter_driver/lib/src/driver/vmservice_driver.dart b/packages/flutter_driver/lib/src/driver/vmservice_driver.dart
index c275175bed..ec76c97de1 100644
--- a/packages/flutter_driver/lib/src/driver/vmservice_driver.dart
+++ b/packages/flutter_driver/lib/src/driver/vmservice_driver.dart
@@ -100,6 +100,19 @@ class VMServiceFlutterDriver extends FlutterDriver {
       }
     }
 
+    // Refreshes the isolate state periodically until the isolate reports as
+    // being runnable.
+    Future<vms.Isolate> waitForIsolateToBeRunnable(vms.IsolateRef ref) async {
+      while (true) {
+        final vms.Isolate isolate = await client.getIsolate(ref.id!);
+        if (isolate.pauseEvent!.kind == vms.EventKind.kNone) {
+          await Future<void>.delayed(_kPauseBetweenIsolateRefresh);
+        } else {
+          return isolate;
+        }
+      }
+    }
+
     final vms.IsolateRef isolateRef = (await _warnIfSlow<vms.IsolateRef?>(
       future: waitForRootIsolate(),
       timeout: kUnusuallyLongTimeout,
@@ -108,11 +121,13 @@ class VMServiceFlutterDriver extends FlutterDriver {
         : 'Isolate $isolateNumber is taking an unusually long time to start.',
     ))!;
     _log('Isolate found with number: ${isolateRef.number}');
-    vms.Isolate isolate = await client.getIsolate(isolateRef.id!);
-
-    if (isolate.pauseEvent!.kind == vms.EventKind.kNone) {
-      isolate = await client.getIsolate(isolateRef.id!);
-    }
+    final vms.Isolate isolate = await _warnIfSlow<vms.Isolate>(
+      future: waitForIsolateToBeRunnable(isolateRef),
+      timeout: kUnusuallyLongTimeout,
+      message: 'The isolate ${isolateRef.number} is taking unusually long time '
+          'to initialize. It still reports ${vms.EventKind.kNone} as pause '
+          'event which is incorrect.',
+    );
 
     final VMServiceFlutterDriver driver = VMServiceFlutterDriver.connectedTo(
       client,
@@ -201,7 +216,8 @@ class VMServiceFlutterDriver extends FlutterDriver {
     } else if (isolate.pauseEvent!.kind == vms.EventKind.kPauseExit ||
         isolate.pauseEvent!.kind == vms.EventKind.kPauseBreakpoint ||
         isolate.pauseEvent!.kind == vms.EventKind.kPauseException ||
-        isolate.pauseEvent!.kind == vms.EventKind.kPauseInterrupted) {
+        isolate.pauseEvent!.kind == vms.EventKind.kPauseInterrupted ||
+        isolate.pauseEvent!.kind == vms.EventKind.kPausePostRequest) {
       // If the isolate is paused for any other reason, assume the extension is
       // already there.
       _log('Isolate is paused mid-flight.');
@@ -583,6 +599,9 @@ Future<vms.VmService> _waitAndConnect(String url, Map<String, dynamic>? headers)
 /// the VM service.
 const Duration _kPauseBetweenReconnectAttempts = Duration(seconds: 1);
 
+/// The amount of time we wait prior to refreshing the isolate state.
+const Duration _kPauseBetweenIsolateRefresh = Duration(milliseconds: 100);
+
 // See `timeline_streams` in
 // https://github.com/dart-lang/sdk/blob/main/runtime/vm/timeline.cc
 List<String> _timelineStreamsToString(List<TimelineStream> streams) {
diff --git a/packages/flutter_driver/test/src/real_tests/flutter_driver_test.dart b/packages/flutter_driver/test/src/real_tests/flutter_driver_test.dart
index c8076aebc4..894c280b71 100644
--- a/packages/flutter_driver/test/src/real_tests/flutter_driver_test.dart
+++ b/packages/flutter_driver/test/src/real_tests/flutter_driver_test.dart
@@ -189,6 +189,33 @@ void main() {
       );
     });
 
+    test('Refreshes isolate if it is not started for long time', () async {
+      fakeIsolate.pauseEvent = vms.Event(kind: vms.EventKind.kNone, timestamp: 0);
+      fakeClient.onGetIsolate = changeIsolateEventAfter(
+        5,
+        vms.Event(kind: vms.EventKind.kPauseStart, timestamp: 1),
+      );
+
+      final FlutterDriver driver = await FlutterDriver.connect(dartVmServiceUrl: '');
+      expect(driver, isNotNull);
+      expect(
+        fakeClient.connectionLog,
+        <String>[
+          'getIsolate',
+          'getIsolate',
+          'getIsolate',
+          'getIsolate',
+          'getIsolate',
+          'setFlag pause_isolates_on_start false',
+          'resume',
+          'streamListen Isolate',
+          'getIsolate',
+          'onIsolateEvent',
+          'streamCancel Isolate',
+        ],
+      );
+    });
+
     test('Connects to isolate number', () async {
       fakeIsolate.pauseEvent = vms.Event(kind: vms.EventKind.kPauseStart, timestamp: 0);
       final FlutterDriver driver = await FlutterDriver.connect(dartVmServiceUrl: '', isolateNumber: int.parse(fakeIsolate.number!));
@@ -246,6 +273,14 @@ void main() {
       expectLogContains('Isolate is paused mid-flight');
     });
 
+    test('connects to isolate paused mid-flight after request', () async {
+      fakeIsolate.pauseEvent = vms.Event(kind: vms.EventKind.kPausePostRequest, timestamp: 0);
+
+      final FlutterDriver driver = await FlutterDriver.connect(dartVmServiceUrl: '');
+      expect(driver, isNotNull);
+      expectLogContains('Isolate is paused mid-flight');
+    });
+
     // This test simulates a situation when we believe that the isolate is
     // currently paused, but something else (e.g. a debugger) resumes it before
     // we do. There's no need to fail as we should be able to drive the app
@@ -1055,6 +1090,15 @@ vms.Response? makeFakeResponse(
   });
 }
 
+void Function(vms.Isolate) changeIsolateEventAfter(int gets, vms.Event nextEvent) {
+  return (vms.Isolate i) {
+    gets -= 1;
+    if (gets == 0) {
+      i.pauseEvent = nextEvent;
+    }
+  };
+}
+
 class FakeFlutterWebConnection extends Fake implements FlutterWebConnection {
   @override
   bool supportsTimelineAction = false;
@@ -1082,6 +1126,7 @@ class FakeVmService extends Fake implements vms.VmService {
   FakeVM? vm;
   bool failOnSetFlag = false;
   bool failOnResumeWith101 = false;
+  void Function(vms.Isolate)? onGetIsolate;
 
   final List<String> connectionLog = <String>[];
 
@@ -1092,6 +1137,7 @@ class FakeVmService extends Fake implements vms.VmService {
   Future<vms.Isolate> getIsolate(String isolateId) async {
     connectionLog.add('getIsolate');
     if (isolateId == vm!.isolate!.id) {
+      onGetIsolate?.call(vm!.isolate!);
       return vm!.isolate!;
     }
     throw UnimplementedError('getIsolate called with unrecognized $isolateId');