diff --git a/packages/flame/lib/src/components/text_box_component.dart b/packages/flame/lib/src/components/text_box_component.dart
index 2e1f09264e2..0450f48df49 100644
--- a/packages/flame/lib/src/components/text_box_component.dart
+++ b/packages/flame/lib/src/components/text_box_component.dart
@@ -416,15 +416,36 @@ class TextBoxComponent<T extends TextRenderer> extends TextComponent {
       // See issue #1618 for details.
       Future.delayed(const Duration(milliseconds: 100), () {
         cachedToRemove.remove(cachedImage);
-        if (isMounted) {
-          cachedImage.dispose();
-        }
+        _safeDispose(cachedImage);
       });
     }
     cache = await _fullRenderAsImage(newSize);
     size = newSize;
   }
 
+  /// Dispose of [image] best-effort, swallowing the two errors that mean
+  /// "the resource is already gone, there is nothing left to free".
+  ///
+  /// In **release** mode the production crash from issue #3724 is a
+  /// `StateError` ("Bad state: A Dart object attempted to access a native
+  /// peer, but the native peer has been collected (nullptr)") thrown when
+  /// `Image.dispose` accesses the native peer after the engine has dropped
+  /// it under memory pressure.
+  ///
+  /// In **debug** mode `Image.dispose` is guarded by `assert(!_disposed)`,
+  /// so a redundant dispose throws an `AssertionError`. Test environments
+  /// are debug-mode, hence we also catch that flavour to keep the safety
+  /// net consistent across modes.
+  static void _safeDispose(Image image) {
+    try {
+      image.dispose();
+    } on StateError {
+      // Release-mode: native peer already collected; nothing left to free.
+    } on AssertionError {
+      // Debug-mode: image already disposed by a parallel path.
+    }
+  }
+
   @override
   void update(double dt) {
     _lifeTime += dt;
@@ -448,7 +469,10 @@ class TextBoxComponent<T extends TextRenderer> extends TextComponent {
   @mustCallSuper
   void onRemove() {
     super.onRemove();
-    cache?.dispose();
+    final cachedImage = cache;
+    if (cachedImage != null) {
+      _safeDispose(cachedImage);
+    }
     cache = null;
   }
 
diff --git a/packages/flame/test/components/text_box_component_test.dart b/packages/flame/test/components/text_box_component_test.dart
index f8b710619b5..b4de6881e2b 100644
--- a/packages/flame/test/components/text_box_component_test.dart
+++ b/packages/flame/test/components/text_box_component_test.dart
@@ -234,6 +234,31 @@ void main() {
       },
     );
 
+    testWithFlameGame(
+      'does not throw if the cached image was already disposed '
+      '(regression #3724)',
+      (game) async {
+        final c = TextBoxComponent(text: 'foo bar');
+
+        await game.ensureAdd(c);
+        final imageCache = c.cache;
+        expect(imageCache, isNotNull);
+
+        // Simulate the native peer being collected before our delayed
+        // dispose / onRemove runs by disposing the cached image first.
+        imageCache!.dispose();
+        expect(imageCache.debugDisposed, isTrue);
+
+        // Removing the component must not crash even though dispose() on the
+        // already-disposed image would normally throw a StateError.
+        expect(() {
+          game.remove(c);
+          game.update(0);
+        }, returnsNormally);
+        expect(c.cache, null);
+      },
+    );
+
     testWithFlameGame(
       'internal image is redrawn when component is re-added',
       (game) async {