diff --git a/homeassistant/helpers/aiohttp_client.py b/homeassistant/helpers/aiohttp_client.py
index 3d8dc247857..a9976cf7e32 100644
--- a/homeassistant/helpers/aiohttp_client.py
+++ b/homeassistant/helpers/aiohttp_client.py
@@ -28,6 +28,7 @@ from homeassistant.util.json import json_loads
 
 from .frame import warn_use
 from .json import json_dumps
+from .singleton import singleton
 
 if TYPE_CHECKING:
     from aiohttp.typedefs import JSONDecoder
@@ -39,6 +40,7 @@ DATA_CONNECTOR: HassKey[dict[tuple[bool, int, str], aiohttp.BaseConnector]] = Ha
 DATA_CLIENTSESSION: HassKey[dict[tuple[bool, int, str], aiohttp.ClientSession]] = (
     HassKey("aiohttp_clientsession")
 )
+DATA_RESOLVER: HassKey[HassAsyncDNSResolver] = HassKey("aiohttp_resolver")
 
 SERVER_SOFTWARE = (
     f"{APPLICATION_NAME}/{__version__} "
@@ -70,6 +72,21 @@ MAXIMUM_CONNECTIONS = 4096
 MAXIMUM_CONNECTIONS_PER_HOST = 100
 
 
+class HassAsyncDNSResolver(AsyncDualMDNSResolver):
+    """Home Assistant AsyncDNSResolver.
+
+    This is a wrapper around the AsyncDualMDNSResolver to only
+    close the resolver when the Home Assistant instance is closed.
+    """
+
+    async def real_close(self) -> None:
+        """Close the resolver."""
+        await super().close()
+
+    async def close(self) -> None:
+        """Close the resolver."""
+
+
 class HassClientResponse(aiohttp.ClientResponse):
     """aiohttp.ClientResponse with a json method that uses json_loads by default."""
 
@@ -363,7 +380,7 @@ def _async_get_connector(
         ssl=ssl_context,
         limit=MAXIMUM_CONNECTIONS,
         limit_per_host=MAXIMUM_CONNECTIONS_PER_HOST,
-        resolver=_async_make_resolver(hass),
+        resolver=_async_get_or_create_resolver(hass),
     )
     connectors[connector_key] = connector
 
@@ -376,6 +393,19 @@ def _async_get_connector(
     return connector
 
 
+@singleton(DATA_RESOLVER)
 @callback
-def _async_make_resolver(hass: HomeAssistant) -> AsyncDualMDNSResolver:
-    return AsyncDualMDNSResolver(async_zeroconf=zeroconf.async_get_async_zeroconf(hass))
+def _async_get_or_create_resolver(hass: HomeAssistant) -> HassAsyncDNSResolver:
+    """Return the HassAsyncDNSResolver."""
+    resolver = _async_make_resolver(hass)
+
+    async def _async_close_resolver(event: Event) -> None:
+        await resolver.real_close()
+
+    hass.bus.async_listen_once(EVENT_HOMEASSISTANT_CLOSE, _async_close_resolver)
+    return resolver
+
+
+@callback
+def _async_make_resolver(hass: HomeAssistant) -> HassAsyncDNSResolver:
+    return HassAsyncDNSResolver(async_zeroconf=zeroconf.async_get_async_zeroconf(hass))
diff --git a/tests/conftest.py b/tests/conftest.py
index ff4a09096e0..9b861d5bde5 100644
--- a/tests/conftest.py
+++ b/tests/conftest.py
@@ -1319,9 +1319,11 @@ def disable_translations_once(
 @pytest_asyncio.fixture(autouse=True, scope="session", loop_scope="session")
 async def mock_zeroconf_resolver() -> AsyncGenerator[_patch]:
     """Mock out the zeroconf resolver."""
+    resolver = AsyncResolver()
+    resolver.real_close = resolver.close
     patcher = patch(
         "homeassistant.helpers.aiohttp_client._async_make_resolver",
-        return_value=AsyncResolver(),
+        return_value=resolver,
     )
     patcher.start()
     try:
diff --git a/tests/helpers/test_aiohttp_client.py b/tests/helpers/test_aiohttp_client.py
index 6d2a7e7a8bb..e44111634d1 100644
--- a/tests/helpers/test_aiohttp_client.py
+++ b/tests/helpers/test_aiohttp_client.py
@@ -401,3 +401,15 @@ async def test_async_mdnsresolver(
     resp = await session.post("http://localhost/xyz", json={"x": 1})
     assert resp.status == 200
     assert await resp.json() == {"x": 1}
+
+
+async def test_resolver_is_singleton(hass: HomeAssistant) -> None:
+    """Test that the resolver is a singleton."""
+    session = client.async_get_clientsession(hass)
+    session2 = client.async_get_clientsession(hass)
+    session3 = client.async_create_clientsession(hass)
+    assert isinstance(session._connector, aiohttp.TCPConnector)
+    assert isinstance(session2._connector, aiohttp.TCPConnector)
+    assert isinstance(session3._connector, aiohttp.TCPConnector)
+    assert session._connector._resolver is session2._connector._resolver
+    assert session._connector._resolver is session3._connector._resolver