diff --git a/airflow-core/tests/conftest.py b/airflow-core/tests/conftest.py
index bffa1c61e8912..b4e3e66b6bdaf 100644
--- a/airflow-core/tests/conftest.py
+++ b/airflow-core/tests/conftest.py
@@ -161,3 +161,12 @@ def requests_mock() -> RequestsMockFixture: ...
     # time-machine
     @pytest.fixture  # type: ignore[no-redef]
     def time_machine() -> TimeMachineFixture: ...
+
+
+@pytest.fixture(autouse=True)
+def _clear_in_process_api_cache():
+    """Clear the cached InProcessExecutionAPI after each test to prevent state leakage."""
+    yield
+    supervisor_module = sys.modules.get("airflow.sdk.execution_time.supervisor")
+    if supervisor_module is not None:
+        supervisor_module.in_process_api_server.cache_clear()
diff --git a/task-sdk/src/airflow/sdk/execution_time/supervisor.py b/task-sdk/src/airflow/sdk/execution_time/supervisor.py
index 8675305dde967..b34d17e0bc3b6 100644
--- a/task-sdk/src/airflow/sdk/execution_time/supervisor.py
+++ b/task-sdk/src/airflow/sdk/execution_time/supervisor.py
@@ -21,6 +21,7 @@
 
 import atexit
 import contextlib
+import functools
 import io
 import logging
 import os
@@ -1531,6 +1532,7 @@ def _send_new_log_fd(self, req_id: int) -> None:
         child_logs.close()  # Close this end now.
 
 
+@functools.lru_cache(maxsize=1)
 def in_process_api_server():
     from airflow.api_fastapi.execution_api.app import InProcessExecutionAPI
 
@@ -1692,8 +1694,9 @@ def start(  # type: ignore[override]
     @staticmethod
     def _api_client(dag=None):
         api = in_process_api_server()
+        from airflow.api_fastapi.common.dagbag import dag_bag_from_app
+
         if dag is not None:
-            from airflow.api_fastapi.common.dagbag import dag_bag_from_app
             from airflow.models.dagbag import DBDagBag
 
             # This is needed since the Execution API server uses the DBDagBag in its "state".
@@ -1701,6 +1704,8 @@ def _api_client(dag=None):
             dag_bag = DBDagBag()
 
             api.app.dependency_overrides[dag_bag_from_app] = lambda: dag_bag
+        else:
+            api.app.dependency_overrides.pop(dag_bag_from_app, None)
 
         client = InProcessTestSupervisor._Client(
             base_url=None, token="", dry_run=True, transport=api.transport
diff --git a/task-sdk/tests/task_sdk/execution_time/test_supervisor.py b/task-sdk/tests/task_sdk/execution_time/test_supervisor.py
index e88b5c794cfda..33271d1f8f3f6 100644
--- a/task-sdk/tests/task_sdk/execution_time/test_supervisor.py
+++ b/task-sdk/tests/task_sdk/execution_time/test_supervisor.py
@@ -141,6 +141,7 @@
     InProcessTestSupervisor,
     _make_process_nondumpable,
     _remote_logging_conn,
+    in_process_api_server,
     process_log_messages_from_subprocess,
     set_supervisor_comms,
     supervise,
@@ -3297,3 +3298,39 @@ def test_nondumpable_noop_on_non_linux():
     """On non-Linux, _make_process_nondumpable returns without error."""
 
     _make_process_nondumpable()
+
+
+def test_in_process_api_server_caches_instance():
+    """in_process_api_server() returns the same instance on repeated calls."""
+    in_process_api_server.cache_clear()
+    try:
+        first = in_process_api_server()
+        second = in_process_api_server()
+        assert first is second
+
+        in_process_api_server.cache_clear()
+        third = in_process_api_server()
+        assert third is not first
+    finally:
+        in_process_api_server.cache_clear()
+
+
+def test_api_client_clears_dag_bag_override_when_dag_is_none():
+    """_api_client(dag=None) removes stale dag_bag_from_app overrides set by a previous call."""
+    from unittest.mock import MagicMock
+
+    from airflow.api_fastapi.common.dagbag import dag_bag_from_app
+
+    in_process_api_server.cache_clear()
+    try:
+        # First call with a dag sets the override
+        mock_dag = MagicMock()
+        InProcessTestSupervisor._api_client(dag=mock_dag)
+        api = in_process_api_server()
+        assert dag_bag_from_app in api.app.dependency_overrides
+
+        # Second call with dag=None should remove it
+        InProcessTestSupervisor._api_client(dag=None)
+        assert dag_bag_from_app not in api.app.dependency_overrides
+    finally:
+        in_process_api_server.cache_clear()