diff --git a/packages/flutter_tools/lib/src/base/error_handling_io.dart b/packages/flutter_tools/lib/src/base/error_handling_io.dart
index 41bc27e8859..e7086141d92 100644
--- a/packages/flutter_tools/lib/src/base/error_handling_io.dart
+++ b/packages/flutter_tools/lib/src/base/error_handling_io.dart
@@ -124,7 +124,7 @@ class ErrorHandlingFileSystem extends ForwardingFileSystem {
 
   @override
   Directory get systemTempDirectory {
-    return directory(delegate.systemTempDirectory);
+    return _runSync(() => directory(delegate.systemTempDirectory), platform: _platform);
   }
 
   @override
diff --git a/packages/flutter_tools/test/general.shard/base/error_handling_io_test.dart b/packages/flutter_tools/test/general.shard/base/error_handling_io_test.dart
index a43367c3419..c4b661dfaa6 100644
--- a/packages/flutter_tools/test/general.shard/base/error_handling_io_test.dart
+++ b/packages/flutter_tools/test/general.shard/base/error_handling_io_test.dart
@@ -884,7 +884,7 @@ void main() {
     });
   });
 
-  testWithoutContext("ErrorHandlingFileSystem.systemTempDirectory wraps delegates filesystem's systemTempDirectory", () {
+  testWithoutContext("ErrorHandlingFileSystem.systemTempDirectory wraps delegate filesystem's systemTempDirectory", () {
     final FileExceptionHandler exceptionHandler = FileExceptionHandler();
 
     final MemoryFileSystem delegate = MemoryFileSystem.test(
@@ -921,6 +921,35 @@ Please ensure that the SDK and/or project is installed in a location that has re
     );
   });
 
+  testWithoutContext("ErrorHandlingFileSystem.systemTempDirectory handles any exception thrown by the delegate's systemTempDirectory implementation", () {
+    final FileExceptionHandler exceptionHandler = FileExceptionHandler();
+    exceptionHandler.addTempError(
+      FileSystemOp.create,
+      const FileSystemException(
+        'Creation of temporary directory failed',
+        'some/temp/path',
+        OSError(
+          'No space left on device',
+          28,
+        ),
+      ),
+    );
+
+    final MemoryFileSystem delegate = MemoryFileSystem.test(
+      opHandle: exceptionHandler.opHandle,
+    );
+
+    final FileSystem fs = ErrorHandlingFileSystem(
+      delegate: delegate,
+      platform: FakePlatform(),
+    );
+
+    expect(
+      () => fs.systemTempDirectory,
+      throwsToolExit(message: 'Free up space and try again.'),
+    );
+  });
+
   group('ProcessManager on windows throws tool exit', () {
     const int kDeviceFull = 112;
     const int kUserMappedSectionOpened = 1224;