diff --git a/packages/flutter_tools/lib/src/ios/devices.dart b/packages/flutter_tools/lib/src/ios/devices.dart
index 58415c06b313b..4d1e5db082e28 100644
--- a/packages/flutter_tools/lib/src/ios/devices.dart
+++ b/packages/flutter_tools/lib/src/ios/devices.dart
@@ -39,6 +39,24 @@ import 'xcode_build_settings.dart';
 import 'xcode_debug.dart';
 import 'xcodeproj.dart';
 
+const String kJITCrashFailureMessage =
+    'Crash occurred when compiling unknown function in unoptimized JIT mode in unknown pass';
+
+@visibleForTesting
+String jITCrashFailureInstructions(String deviceVersion) => '''
+════════════════════════════════════════════════════════════════════════════════
+A change to iOS has caused a temporary break in Flutter's debug mode on
+physical devices.
+See https://github.com/flutter/flutter/issues/163984 for details.
+
+In the meantime, we recommend these temporary workarounds:
+
+* When developing with a physical device, use one running iOS 18.3 or lower.
+* Use a simulator for development rather than a physical device.
+* If you must use a device updated to $deviceVersion, use Flutter's release or
+  profile mode via --release or --profile flags.
+════════════════════════════════════════════════════════════════════════════════''';
+
 class IOSDevices extends PollingDeviceDiscovery {
   IOSDevices({
     required Platform platform,
@@ -594,6 +612,7 @@ class IOSDevice extends Device {
           debuggingOptions: debuggingOptions,
           packageId: packageId,
           vmServiceDiscovery: vmServiceDiscovery,
+          package: package,
         );
       } else if (isWirelesslyConnected) {
         // Wait for the Dart VM url to be discovered via logs (from `ios-deploy`)
@@ -702,6 +721,7 @@ class IOSDevice extends Device {
     required String packageId,
     required DebuggingOptions debuggingOptions,
     ProtocolDiscovery? vmServiceDiscovery,
+    IOSApp? package,
   }) async {
     Timer? maxWaitForCI;
     final Completer<Uri?> cancelCompleter = Completer<Uri?>();
@@ -743,6 +763,11 @@ class IOSDevice extends Device {
       });
     }
 
+    final StreamSubscription<String>? errorListener = await _interceptErrorsFromLogs(
+      package,
+      debuggingOptions: debuggingOptions,
+    );
+
     final Future<Uri?> vmUrlFromMDns = MDnsVmServiceDiscovery.instance!.getVMServiceUriForLaunch(
       packageId,
       this,
@@ -771,9 +796,40 @@ class IOSDevice extends Device {
       }
     }
     maxWaitForCI?.cancel();
+    await errorListener?.cancel();
     return localUri;
   }
 
+  /// Listen to device logs for crash on iOS 18.4+ due to JIT restriction. If
+  /// found, give guided error and throw tool exit. Returns null and does not
+  /// listen if device is less than iOS 18.4.
+  Future<StreamSubscription<String>?> _interceptErrorsFromLogs(
+    IOSApp? package, {
+    required DebuggingOptions debuggingOptions,
+  }) async {
+    // Currently only checking for kJITCrashFailureMessage, which only should
+    // be checked on iOS 18.4+.
+    if (sdkVersion == null || sdkVersion! < Version(18, 4, null)) {
+      return null;
+    }
+    final DeviceLogReader deviceLogReader = getLogReader(
+      app: package,
+      usingCISystem: debuggingOptions.usingCISystem,
+    );
+
+    final Stream<String> logStream = deviceLogReader.logLines;
+
+    final String deviceSdkVersion = await sdkNameAndVersion;
+
+    final StreamSubscription<String> errorListener = logStream.listen((String line) {
+      if (line.contains(kJITCrashFailureMessage)) {
+        throwToolExit(jITCrashFailureInstructions(deviceSdkVersion));
+      }
+    });
+
+    return errorListener;
+  }
+
   ProtocolDiscovery _setupDebuggerAndVmServiceDiscovery({
     required IOSApp package,
     required Directory bundle,
diff --git a/packages/flutter_tools/test/general.shard/ios/ios_device_start_prebuilt_test.dart b/packages/flutter_tools/test/general.shard/ios/ios_device_start_prebuilt_test.dart
index 485c3a75f51af..3a6ebb571ac88 100644
--- a/packages/flutter_tools/test/general.shard/ios/ios_device_start_prebuilt_test.dart
+++ b/packages/flutter_tools/test/general.shard/ios/ios_device_start_prebuilt_test.dart
@@ -1101,6 +1101,75 @@ void main() {
           MDnsVmServiceDiscovery: () => FakeMDnsVmServiceDiscovery(returnsNull: true),
         },
       );
+
+      testUsingContext(
+        'IOSDevice.startApp prints guided message when iOS 18.4 crashes due to JIT',
+        () async {
+          final FileSystem fileSystem = MemoryFileSystem.test();
+          final FakeProcessManager processManager = FakeProcessManager.empty();
+
+          final Directory temporaryXcodeProjectDirectory = fileSystem.systemTempDirectory
+              .childDirectory('flutter_empty_xcode.rand0');
+          final Directory bundleLocation = fileSystem.currentDirectory;
+          final IOSDevice device = setUpIOSDevice(
+            sdkVersion: '18.4',
+            processManager: processManager,
+            fileSystem: fileSystem,
+            isCoreDevice: true,
+            coreDeviceControl: FakeIOSCoreDeviceControl(),
+            xcodeDebug: FakeXcodeDebug(
+              expectedProject: XcodeDebugProject(
+                scheme: 'Runner',
+                xcodeWorkspace: temporaryXcodeProjectDirectory.childDirectory('Runner.xcworkspace'),
+                xcodeProject: temporaryXcodeProjectDirectory.childDirectory('Runner.xcodeproj'),
+                hostAppProjectName: 'Runner',
+              ),
+              expectedDeviceId: '123',
+              expectedLaunchArguments: <String>['--enable-dart-profiling'],
+              expectedBundlePath: bundleLocation.path,
+            ),
+          );
+          final IOSApp iosApp = PrebuiltIOSApp(
+            projectBundleId: 'app',
+            bundleName: 'Runner',
+            uncompressedBundle: bundleLocation,
+            applicationPackage: bundleLocation,
+          );
+          final FakeDeviceLogReader deviceLogReader = FakeDeviceLogReader();
+
+          device.portForwarder = const NoOpDevicePortForwarder();
+          device.setLogReader(iosApp, deviceLogReader);
+
+          // Start writing messages to the log reader.
+          Timer.run(() {
+            deviceLogReader.addLine(kJITCrashFailureMessage);
+          });
+
+          final Completer<void> completer = Completer<void>();
+          // device.startApp() asynchronously calls throwToolExit, so we
+          // catch it in a zone.
+          unawaited(
+            runZoned<Future<void>?>(
+              () {
+                unawaited(
+                  device.startApp(
+                    iosApp,
+                    prebuiltApplication: true,
+                    debuggingOptions: DebuggingOptions.enabled(BuildInfo.debug),
+                    platformArgs: <String, dynamic>{},
+                  ),
+                );
+                return null;
+              },
+              onError: (Object error, StackTrace stack) {
+                expect(error.toString(), contains(jITCrashFailureInstructions('iOS 18.4')));
+                completer.complete();
+              },
+            ),
+          );
+          await completer.future;
+        },
+      );
     });
   });
 }