diff --git a/airflow-core/newsfragments/69087.bugfix.rst b/airflow-core/newsfragments/69087.bugfix.rst
new file mode 100644
index 0000000000000..9fd89cb6882c0
--- /dev/null
+++ b/airflow-core/newsfragments/69087.bugfix.rst
@@ -0,0 +1 @@
+Initialize versioned Dag bundles for callback queueing when bundle_version is None (e.g. with disable_bundle_versioning=True), so callbacks resolve a usable bundle path instead of an uninitialized one.
diff --git a/airflow-core/src/airflow/dag_processing/manager.py b/airflow-core/src/airflow/dag_processing/manager.py
index b2428985a6506..ce5dace5fde5d 100644
--- a/airflow-core/src/airflow/dag_processing/manager.py
+++ b/airflow-core/src/airflow/dag_processing/manager.py
@@ -701,22 +701,24 @@ def prepare_callback_bundle(self, request: CallbackRequest) -> BaseDagBundle | N
         Return the bundle to run the callback against, or ``None`` to skip the callback.
 
         Default implementation looks the bundle up via :class:`DagBundlesManager` and, for
-        versioned requests on bundles that support versioning, calls ``bundle.initialize()``.
-        Override to source the bundle from an API.
+        bundles that support versioning, calls ``bundle.initialize()`` so ``bundle.path`` is
+        resolved before the caller reads it. This happens even when ``request.bundle_version``
+        is ``None`` (e.g. ``disable_bundle_versioning=True``), in which case the bundle resolves
+        its current effective version. Override to source the bundle from an API.
         """
         try:
             bundle = DagBundlesManager().get_bundle(name=request.bundle_name, version=request.bundle_version)
         except ValueError:
             self.log.error("Bundle %s no longer configured, skipping callback", request.bundle_name)
             return None
-        if bundle.supports_versioning and request.bundle_version:
+        if bundle.supports_versioning:
             try:
                 bundle.initialize()
             except Exception:
                 self.log.exception(
                     "Error initializing bundle %s version %s for callback, skipping",
                     request.bundle_name,
-                    request.bundle_version,
+                    request.bundle_version if request.bundle_version is not None else "latest",
                 )
                 return None
         return bundle
diff --git a/airflow-core/tests/unit/dag_processing/test_manager.py b/airflow-core/tests/unit/dag_processing/test_manager.py
index 4b55b6b2f1ee9..b5ace87c04b5e 100644
--- a/airflow-core/tests/unit/dag_processing/test_manager.py
+++ b/airflow-core/tests/unit/dag_processing/test_manager.py
@@ -1967,7 +1967,9 @@ def test_prepare_callback_bundle_initializes_versioned_bundle(self, mock_bundle_
         bundle.initialize.assert_called_once()
 
     @mock.patch("airflow.dag_processing.manager.DagBundlesManager")
-    def test_prepare_callback_bundle_skips_initialize_for_unversioned_request(self, mock_bundle_manager):
+    def test_prepare_callback_bundle_initializes_versioned_bundle_when_version_is_none(
+        self, mock_bundle_manager
+    ):
         manager = DagFileProcessorManager(max_runs=1)
         bundle = MagicMock(spec=BaseDagBundle)
         bundle.supports_versioning = True
@@ -1984,7 +1986,7 @@ def test_prepare_callback_bundle_skips_initialize_for_unversioned_request(self,
         )
 
         assert manager.prepare_callback_bundle(request) is bundle
-        bundle.initialize.assert_not_called()
+        bundle.initialize.assert_called_once()
 
     @mock.patch("airflow.dag_processing.manager.DagBundlesManager")
     def test_prepare_callback_bundle_skips_initialize_for_non_versioning_bundle(self, mock_bundle_manager):
@@ -2071,6 +2073,34 @@ def test_add_callback_queues_file_info_on_success(self, mock_bundle_manager):
         assert file_info.bundle_name == "testing"
         assert requests == [request]
 
+    @mock.patch("airflow.dag_processing.manager.DagBundlesManager")
+    def test_add_callback_queues_resolved_path_when_version_is_none(self, mock_bundle_manager):
+        manager = DagFileProcessorManager(max_runs=1)
+        initialized_path = Path("/tmp/bundle-initialized")
+        bundle = MagicMock(spec=BaseDagBundle)
+        bundle.supports_versioning = True
+        # A versioned bundle's path is only usable after initialize(); simulate that by
+        # leaving path unresolved until initialize() materializes it.
+        bundle.path = Path("/dev/null")
+        bundle.initialize.side_effect = lambda: setattr(bundle, "path", initialized_path)
+        mock_bundle_manager.return_value.get_bundle.return_value = bundle
+
+        request = DagCallbackRequest(
+            filepath="file1.py",
+            dag_id="dag1",
+            run_id="run1",
+            is_failure_callback=False,
+            bundle_name="testing",
+            bundle_version=None,
+            msg=None,
+        )
+
+        manager._add_callback_to_queue(request)
+
+        bundle.initialize.assert_called_once()
+        [(file_info, _)] = manager._callback_to_execute.items()
+        assert file_info.bundle_path == initialized_path
+
     @mock.patch("airflow.dag_processing.manager.DagBundlesManager")
     def test_add_callback_skips_when_bundle_init_fails(self, mock_bundle_manager):
         manager = DagFileProcessorManager(max_runs=1)