diff --git a/.gitignore b/.gitignore
index f894cace..c4b9f885 100644
--- a/.gitignore
+++ b/.gitignore
@@ -12,6 +12,7 @@
 devtools_options.yaml
 .fvmrc
 .fvm/
+AGENTS.md
 
 # Environment files
 ios/Flutter/Dart-Defines.xcconfig
diff --git a/flutter_cache_manager/CHANGELOG.md b/flutter_cache_manager/CHANGELOG.md
index eb4d067e..97c1a155 100644
--- a/flutter_cache_manager/CHANGELOG.md
+++ b/flutter_cache_manager/CHANGELOG.md
@@ -1,5 +1,6 @@
 ## [Unreleased]
 
+* Fixes `JsonCacheInfoRepository` losing metadata when the app exits within 3 seconds of a cache change by writing through promptly with serialized, atomic file writes ([#491](https://github.com/Baseflow/flutter_cache_manager/issues/491))
 * Modernizes GitHub Actions CI (combined quality job, pinned Flutter 3.44.4, Dependabot for actions)
 * Updates example Android project to AGP 9.0.1 / Gradle 9.1 / Kotlin 2.3.20
 * Migrates example Android app to built-in Kotlin
diff --git a/flutter_cache_manager/lib/src/storage/cache_info_repositories/json_cache_info_repository.dart b/flutter_cache_manager/lib/src/storage/cache_info_repositories/json_cache_info_repository.dart
index e8ee293f..5d24b24a 100644
--- a/flutter_cache_manager/lib/src/storage/cache_info_repositories/json_cache_info_repository.dart
+++ b/flutter_cache_manager/lib/src/storage/cache_info_repositories/json_cache_info_repository.dart
@@ -1,9 +1,9 @@
-import 'dart:async';
 import 'dart:convert';
 import 'dart:io';
 import 'dart:math';
 
 import 'package:collection/collection.dart';
+import 'package:file/file.dart' as pf;
 import 'package:flutter/widgets.dart';
 import 'package:flutter_cache_manager/src/storage/cache_info_repositories/cache_info_repository.dart';
 import 'package:flutter_cache_manager/src/storage/cache_info_repositories/helper_methods.dart';
@@ -31,6 +31,9 @@ class JsonCacheInfoRepository extends CacheInfoRepository
   final Map<String, CacheObject> _cacheObjects = {};
   final Map<int, Map<String, dynamic>> _jsonCache = {};
 
+  bool _dirty = false;
+  Future<void> _writeQueue = Future.value();
+
   @override
   Future<bool> open() async {
     if (!shouldOpenOnNewConnection()) {
@@ -77,7 +80,7 @@ class JsonCacheInfoRepository extends CacheInfoRepository
     if (cacheObject.id == null) {
       throw ArgumentError('Updated objects should have an existing id.');
     }
-    _put(cacheObject, setTouchedToNow);
+    await _put(cacheObject, setTouchedToNow);
     return 1;
   }
 
@@ -104,13 +107,10 @@ class JsonCacheInfoRepository extends CacheInfoRepository
 
   @override
   Future<int> delete(int id) async {
-    final cacheObject = _cacheObjects.values.firstWhereOrNull(
-      (element) => element.id == id,
-    );
-    if (cacheObject == null) {
+    if (!_removeById(id)) {
       return 0;
     }
-    _remove(cacheObject);
+    await _schedulePersist();
     return 1;
   }
 
@@ -118,18 +118,23 @@ class JsonCacheInfoRepository extends CacheInfoRepository
   Future<int> deleteAll(Iterable<int> ids) async {
     var deleted = 0;
     for (final id in ids) {
-      deleted += await delete(id);
+      if (_removeById(id)) deleted++;
+    }
+    if (deleted > 0) {
+      await _schedulePersist();
     }
     return deleted;
   }
 
   @override
   Future<bool> close() async {
-    if (!shouldClose()) {
-      return false;
+    final shouldCloseRepo = shouldClose();
+    if (_dirty) {
+      await _schedulePersist();
+    } else {
+      await _writeQueue;
     }
-    await _saveFile();
-    return true;
+    return shouldCloseRepo;
   }
 
   Future<void> _readFile(File file) async {
@@ -162,33 +167,85 @@ class JsonCacheInfoRepository extends CacheInfoRepository
     }
   }
 
-  CacheObject _put(CacheObject cacheObject, bool setTouchedToNow) {
+  Future<CacheObject> _put(
+    CacheObject cacheObject,
+    bool setTouchedToNow,
+  ) async {
     final map = cacheObject.toMap(setTouchedToNow: setTouchedToNow);
     _jsonCache[cacheObject.id!] = map;
     final updatedCacheObject = CacheObject.fromMap(map);
     _cacheObjects[cacheObject.key] = updatedCacheObject;
-    _cacheUpdated();
+    await _schedulePersist();
     return updatedCacheObject;
   }
 
-  void _remove(CacheObject cacheObject) {
+  bool _removeById(int id) {
+    final cacheObject = _cacheObjects.values.firstWhereOrNull(
+      (element) => element.id == id,
+    );
+    if (cacheObject == null) {
+      return false;
+    }
     _cacheObjects.remove(cacheObject.key);
     _jsonCache.remove(cacheObject.id);
-    _cacheUpdated();
+    return true;
   }
 
-  void _cacheUpdated() {
-    timer?.cancel();
-    timer = Timer(timerDuration, _saveFile);
+  /// Queues a write of the current cache info.
+  ///
+  /// The returned future completes when the changes are on disk. Changes made
+  /// while a write is in progress are written by that same write or the one
+  /// directly after it, so a burst of changes doesn't cause a write per change.
+  Future<void> _schedulePersist() {
+    _dirty = true;
+    _writeQueue = _writeQueue.then((_) => _flushIfDirty());
+    return _writeQueue;
   }
 
-  Timer? timer;
-  Duration timerDuration = const Duration(seconds: 3);
+  Future<void> _flushIfDirty() async {
+    while (_dirty) {
+      _dirty = false;
+      try {
+        await _saveFile();
+      } on Object catch (e, stacktrace) {
+        // Keep the changes dirty so a later change or close retries the write,
+        // but stop here to avoid retrying a persistent failure in a loop.
+        _dirty = true;
+        FlutterError.reportError(
+          FlutterErrorDetails(
+            exception: e,
+            stack: stacktrace,
+            library: 'flutter cache manager',
+            context: ErrorDescription(
+              'Thrown when writing the file containing cache info. '
+              'The cache info could not be persisted and may be lost when the '
+              'app is closed.',
+            ),
+          ),
+        );
+        return;
+      }
+    }
+  }
 
   Future<void> _saveFile() async {
-    timer?.cancel();
-    timer = null;
-    await _file!.writeAsString(jsonEncode(_jsonCache.values.toList()));
+    final file = await _getFile();
+    final content = jsonEncode(_jsonCache.values.toList());
+    final tempFile = _createSiblingFile('${file.path}.tmp');
+    await tempFile.writeAsString(content, flush: true);
+    await tempFile.rename(file.path);
+  }
+
+  /// Creates a file next to [_file] on the same file system.
+  ///
+  /// [_file] can be backed by an alternative [pf.FileSystem], in which case a
+  /// plain [File] would resolve against the local file system instead.
+  File _createSiblingFile(String siblingPath) {
+    final file = _file!;
+    if (file is pf.File) {
+      return file.fileSystem.file(siblingPath);
+    }
+    return File(siblingPath);
   }
 
   @override
@@ -197,6 +254,10 @@ class JsonCacheInfoRepository extends CacheInfoRepository
     if (await file.exists()) {
       await file.delete();
     }
+    final tempFile = _createSiblingFile('${file.path}.tmp');
+    if (await tempFile.exists()) {
+      await tempFile.delete();
+    }
   }
 
   @override
@@ -206,18 +267,20 @@ class JsonCacheInfoRepository extends CacheInfoRepository
   }
 
   Future<File> _getFile() async {
-    if (_file == null) {
-      if (path != null) {
-        directory = File(path!).parent;
-      } else {
-        directory ??= await getApplicationSupportDirectory();
-      }
-      await directory!.create(recursive: true);
-      if (path == null || !path!.endsWith('.json')) {
-        path = join(directory!.path, '$databaseName.json');
-      }
-      _file = File(path!);
+    if (_file != null) {
+      return _file!;
+    }
+
+    if (path != null) {
+      directory = File(path!).parent;
+    } else {
+      directory ??= await getApplicationSupportDirectory();
+    }
+    await directory!.create(recursive: true);
+    if (path == null || !path!.endsWith('.json')) {
+      path = join(directory!.path, '$databaseName.json');
     }
+    _file = File(path!);
     return _file!;
   }
 }
diff --git a/flutter_cache_manager/test/helpers/json_repo_helpers.dart b/flutter_cache_manager/test/helpers/json_repo_helpers.dart
index d31ef552..c725618f 100644
--- a/flutter_cache_manager/test/helpers/json_repo_helpers.dart
+++ b/flutter_cache_manager/test/helpers/json_repo_helpers.dart
@@ -18,13 +18,17 @@ class JsonRepoHelpers {
   static Future<JsonCacheInfoRepository> createRepository({
     bool open = true,
   }) async {
-    var directory = await _createDirectory();
-    var file = await _createFile(directory);
+    var file = await createDatabaseFile();
     var repository = JsonCacheInfoRepository.withFile(file);
     if (open) await repository.open();
     return repository;
   }
 
+  static Future<File> createDatabaseFile() async {
+    var directory = await _createDirectory();
+    return _createFile(directory);
+  }
+
   static Future<Directory> _createDirectory() async {
     var testDir = await MemoryFileSystem().systemTempDirectory.createTemp(
       'testFolder',
diff --git a/flutter_cache_manager/test/repositories/json_file_repository_test.dart b/flutter_cache_manager/test/repositories/json_file_repository_test.dart
index 941738f5..1daf59b6 100644
--- a/flutter_cache_manager/test/repositories/json_file_repository_test.dart
+++ b/flutter_cache_manager/test/repositories/json_file_repository_test.dart
@@ -1,6 +1,8 @@
+import 'dart:convert';
 import 'dart:io';
 
 import 'package:collection/collection.dart';
+import 'package:flutter/foundation.dart';
 import 'package:flutter_cache_manager/src/storage/cache_info_repositories/json_cache_info_repository.dart';
 import 'package:flutter_cache_manager/src/storage/cache_object.dart';
 import 'package:flutter_test/flutter_test.dart';
@@ -230,6 +232,56 @@ void main() {
         JsonRepoHelpers.startCacheObjects.length + 1,
       );
     });
+
+    test('Changes are persisted when the mutating future completes', () async {
+      final file = await JsonRepoHelpers.createDatabaseFile();
+      final repo = JsonCacheInfoRepository.withFile(file);
+      await repo.open();
+      await repo.insert(JsonRepoHelpers.extraCacheObject);
+
+      // New instance reads from disk without closing the first repository.
+      final repo2 = JsonCacheInfoRepository.withFile(file);
+      await repo2.open();
+      final allObjects = await repo2.getAllObjects();
+      expect(allObjects.length, JsonRepoHelpers.startCacheObjects.length + 1);
+    });
+
+    test('Persist does not leave a temp file', () async {
+      final file = await JsonRepoHelpers.createDatabaseFile();
+      final repo = JsonCacheInfoRepository.withFile(file);
+      await repo.open();
+      await repo.insert(JsonRepoHelpers.extraCacheObject);
+
+      final tempFile = file.fileSystem.file('${file.path}.tmp');
+      expect(await tempFile.exists(), false);
+      expect(await file.exists(), true);
+      expect(jsonDecode(await file.readAsString()), isA<List<dynamic>>());
+    });
+
+    test('A failing write is reported and retried on close', () async {
+      final file = await JsonRepoHelpers.createDatabaseFile();
+      final repo = JsonCacheInfoRepository.withFile(file);
+      await repo.open();
+
+      // Writing is impossible while the containing directory is gone.
+      await file.parent.delete(recursive: true);
+
+      final errors = <FlutterErrorDetails>[];
+      final originalOnError = FlutterError.onError;
+      FlutterError.onError = errors.add;
+      await repo.insert(JsonRepoHelpers.extraCacheObject);
+      FlutterError.onError = originalOnError;
+
+      expect(errors, hasLength(1));
+
+      await file.parent.create(recursive: true);
+      expect(await repo.close(), true);
+
+      final repo2 = JsonCacheInfoRepository.withFile(file);
+      await repo2.open();
+      final allObjects = await repo2.getAllObjects();
+      expect(allObjects.length, JsonRepoHelpers.startCacheObjects.length + 1);
+    });
   });
 }