diff --git a/zulip/tests/test_do_api_query.py b/zulip/tests/test_do_api_query.py
new file mode 100644
index 000000000..2b4130047
--- /dev/null
+++ b/zulip/tests/test_do_api_query.py
@@ -0,0 +1,71 @@
+import unittest
+from unittest.mock import MagicMock, patch
+
+import requests
+
+import zulip
+
+
+def make_client() -> zulip.Client:
+    with patch.object(zulip.Client, "call_endpoint") as mock_call:
+        mock_call.return_value = {
+            "result": "success",
+            "zulip_version": "9.0.0",
+            "zulip_feature_level": 300,
+            "msg": "",
+        }
+        client = zulip.Client(
+            email="test@example.com",
+            api_key="deadbeef",
+            site="https://testserver",
+        )
+    return client
+
+
+class TestStaleConnectionRetry(unittest.TestCase):
+    def test_stale_connection_resets_session(self) -> None:
+        client = make_client()
+
+        # Simulate a session that has already been used (has_connected = True)
+        stale_session = MagicMock()
+        client.session = stale_session
+        client.has_connected = True
+
+        # First request raises ConnectionError (stale socket),
+        # second request succeeds
+        success_response = MagicMock()
+        success_response.status_code = 200
+        success_response.json.return_value = {"result": "success", "msg": ""}
+
+        stale_session.request.side_effect = requests.exceptions.ConnectionError("stale")
+
+        fresh_session = MagicMock()
+        fresh_session.request.return_value = success_response
+
+        call_count = 0
+
+        def mock_ensure_session(self: zulip.Client) -> None:
+            nonlocal call_count
+            call_count += 1
+            if call_count == 1:
+                # First call: leave the stale session in place
+                self.session = stale_session
+            else:
+                # Subsequent calls: provide a fresh session
+                self.session = fresh_session
+
+        with patch.object(zulip.Client, "ensure_session", mock_ensure_session):
+            result = client.do_api_query({}, "/api/v1/messages", method="POST")
+
+        # The stale session should have been closed
+        stale_session.close.assert_called_once()
+
+        # The result should come from the fresh session
+        self.assertEqual(result, {"result": "success", "msg": ""})
+
+        # ensure_session should have been called twice (once per loop iteration)
+        self.assertEqual(call_count, 2)
+
+
+if __name__ == "__main__":
+    unittest.main()
diff --git a/zulip/zulip/__init__.py b/zulip/zulip/__init__.py
index 82190a51d..03a5fcb2a 100644
--- a/zulip/zulip/__init__.py
+++ b/zulip/zulip/__init__.py
@@ -600,9 +600,6 @@ def do_api_query(
 
         req_files = [(f.name, f) for f in files]
 
-        self.ensure_session()
-        assert self.session is not None
-
         query_state: Dict[str, Any] = {
             "had_error_retry": False,
             "request": request,
@@ -637,6 +634,9 @@ def end_error_retry(succeeded: bool) -> None:
                     print("Failed!")
 
         while True:
+            self.ensure_session()
+            assert self.session is not None
+
             try:
                 kwarg = "params" if method == "GET" else "data"
 
@@ -686,6 +686,9 @@ def end_error_retry(succeeded: bool) -> None:
                     raise UnrecoverableNetworkError(
                         "cannot connect to server " + self.base_url
                     ) from e
+                if self.session is not None:
+                    self.session.close()
+                    self.session = None
 
                 if error_retry(""):
                     continue