diff --git a/tests/test_xqueue_client.py b/tests/test_xqueue_client.py
index 24cee9d..f57e6e7 100644
--- a/tests/test_xqueue_client.py
+++ b/tests/test_xqueue_client.py
@@ -3,6 +3,7 @@
 import json
 import collections
 import requests
+import requests.cookies
 import requests.exceptions
 
 from xqueue_watcher import client
@@ -20,6 +21,8 @@ def __init__(self):
         self._fail = False
         self._url_checker = None
         self._open = True
+        self.cookies = requests.cookies.RequestsCookieJar()
+        self.headers = {}
 
     def close(self):
         self._open = False
@@ -152,8 +155,17 @@ def login(url, response, session):
         self.session._url_checker = login
 
         reply = self.client.process_one()
-        req = self.session._requests[1]
-        self.assertTrue(req.url, 'TEST/xqueue/login/')
+        # _requests[0]: original GET /xqueue/get_submission/ → 302
+        # _requests[1]: GET /xqueue/login/ (CSRF prefetch)
+        # _requests[2]: POST /xqueue/login/
+        # _requests[3]: retry GET /xqueue/get_submission/ → 200
+        get_csrf_req = self.session._requests[1]
+        self.assertEqual(get_csrf_req.method, 'get')
+        self.assertEqual(get_csrf_req.url, 'TEST/xqueue/login/')
+        post_login_req = self.session._requests[2]
+        self.assertEqual(post_login_req.method, 'post')
+        self.assertEqual(post_login_req.url, 'TEST/xqueue/login/')
+        self.assertEqual(post_login_req.kwargs['headers']['Referer'], 'TEST/xqueue/login/')
         self.assertTrue(reply)
 
     def test_bad_login(self):
@@ -169,10 +181,158 @@ def login(url, response, session):
         self.session._url_checker = login
 
         reply = self.client.process_one()
-        req = self.session._requests[1]
-        self.assertTrue(req.url, 'TEST/xqueue/login/')
+        post_login_req = self.session._requests[2]
+        self.assertEqual(post_login_req.method, 'post')
+        self.assertEqual(post_login_req.url, 'TEST/xqueue/login/')
         self.assertFalse(reply)
 
+    def test_login_sets_referer_header(self):
+        """POST to login always includes Referer pointing at the login URL."""
+        self.session._json = {'return_code': 0, 'msg': 'logged in'}
+        self.client._login()
+        post_req = self.session._requests[1]
+        self.assertEqual(post_req.method, 'post')
+        self.assertEqual(post_req.kwargs['headers']['Referer'], 'TEST/xqueue/login/')
+
+    def test_login_sets_csrf_token_header(self):
+        """X-CSRFToken is set on the POST when the CSRF cookie is present."""
+        def set_csrf_cookie(url, response, session):
+            if url.endswith('xqueue/login/'):
+                session.cookies.set('csrftoken', 'testcsrf123')
+                response.status_code = 200
+                response.json.return_value = {'return_code': 0, 'msg': 'logged in'}
+        self.session._url_checker = set_csrf_cookie
+        self.client._login()
+        post_req = self.session._requests[1]
+        self.assertEqual(post_req.method, 'post')
+        self.assertEqual(post_req.kwargs['headers']['X-CSRFToken'], 'testcsrf123')
+
+    def test_login_sets_edx_csrf_token_header(self):
+        """X-CSRFToken falls back to the edx-csrftoken cookie name."""
+        def set_edx_csrf_cookie(url, response, session):
+            if url.endswith('xqueue/login/'):
+                session.cookies.set('edx-csrftoken', 'edxcsrf456')
+                response.status_code = 200
+                response.json.return_value = {'return_code': 0, 'msg': 'logged in'}
+        self.session._url_checker = set_edx_csrf_cookie
+        self.client._login()
+        post_req = self.session._requests[1]
+        self.assertEqual(post_req.kwargs['headers']['X-CSRFToken'], 'edxcsrf456')
+
+    def test_login_no_csrf_token_header_when_no_cookie(self):
+        """X-CSRFToken is omitted from the POST when no CSRF cookie is available."""
+        self.session._json = {'return_code': 0, 'msg': 'logged in'}
+        self.client._login()
+        post_req = self.session._requests[1]
+        self.assertNotIn('X-CSRFToken', post_req.kwargs['headers'])
+
+    def test_login_clears_stale_session(self):
+        """Stale cookies and X-CSRFToken header are cleared before the CSRF GET."""
+        self.session._json = {'return_code': 0, 'msg': 'logged in'}
+        self.session.cookies.set('sessionid', 'stale_session')
+        self.session.headers['X-CSRFToken'] = 'stale_token'
+        self.client._login()
+        self.assertIsNone(self.session.cookies.get('sessionid'))
+        self.assertNotIn('X-CSRFToken', self.session.headers)
+
+    def test_login_persists_csrf_in_session_headers(self):
+        """After a successful login, the session X-CSRFToken header is updated."""
+        def set_cookie_on_post(url, response, session):
+            if url.endswith('xqueue/login/') and response.status_code == 200:
+                session.cookies.set('csrftoken', 'post_login_csrf')
+                response.json.return_value = {'return_code': 0}
+
+        self.session._url_checker = set_cookie_on_post
+        self.client._login()
+        self.assertEqual(self.session.headers.get('X-CSRFToken'), 'post_login_csrf')
+
+    def test_login_persists_referer_in_session_headers(self):
+        """After login, Referer is set in session headers so POST requests pass
+        Django's HTTPS Referer check (required by Django 4+ CSRF enforcement)."""
+        self.session._json = {'return_code': 0, 'msg': 'logged in'}
+        self.client._login()
+        self.assertEqual(self.session.headers.get('Referer'), self.client.xqueue_server)
+
+    def test_reauth_only_once_per_request(self):
+        """Re-authentication is attempted at most once; persistent failures return False."""
+        self.client.add_handler(self._simple_handler)
+        login_call_count = [0]
+
+        def always_auth_error(url, response, session):
+            if url.endswith('xqueue/login/'):
+                login_call_count[0] += 1
+                response.status_code = 200
+                response.json.return_value = {'return_code': 0, 'msg': 'logged in'}
+            else:
+                response.status_code = 403
+
+        self.session._url_checker = always_auth_error
+        self.session.status_code = 403
+
+        reply = self.client.process_one()
+        self.assertFalse(reply)
+        # _login() makes GET + POST = 2 requests to the login URL, but only once
+        self.assertEqual(login_call_count[0], 2)
+
+    def test_reauth_on_401(self):
+        """A 401 response triggers re-authentication just like a 302 redirect."""
+        self.client.add_handler(self._simple_handler)
+        self.session.status_code = 401
+
+        def login(url, response, session):
+            if url.endswith('xqueue/login/'):
+                response.status_code = 200
+                response.json.return_value = {'return_code': 0, 'msg': 'logged in'}
+                session.status_code = 200
+        self.session._url_checker = login
+
+        reply = self.client.process_one()
+        self.assertTrue(reply)
+
+    def test_reauth_on_403(self):
+        """A 403 response (e.g. CSRF failure) triggers re-authentication."""
+        self.client.add_handler(self._simple_handler)
+        self.session.status_code = 403
+
+        def login(url, response, session):
+            if url.endswith('xqueue/login/'):
+                response.status_code = 200
+                response.json.return_value = {'return_code': 0, 'msg': 'logged in'}
+                session.status_code = 200
+        self.session._url_checker = login
+
+        reply = self.client.process_one()
+        self.assertTrue(reply)
+
+    def test_put_result_reauth_with_csrf(self):
+        """When put_result returns 403 (CSRF failure), re-auth obtains a fresh
+        CSRF token via the GET /xqueue/login/ endpoint and the retry succeeds."""
+        put_result_attempts = [0]
+
+        def handler(content):
+            return {'result': True}
+        self.client.add_handler(handler)
+
+        def url_checker(url, response, session):
+            if url.endswith('xqueue/login/'):
+                session.cookies.set('csrftoken', 'fresh_csrf_token')
+                response.status_code = 200
+                response.json.return_value = {'return_code': 0, 'content': ''}
+            elif url.endswith('put_result/'):
+                put_result_attempts[0] += 1
+                if put_result_attempts[0] == 1:
+                    response.status_code = 403
+                else:
+                    response.status_code = 200
+                    response.json.return_value = {'return_code': 0, 'content': ''}
+
+        self.session._url_checker = url_checker
+        result = self.client.process_one()
+
+        self.assertTrue(result)
+        self.assertEqual(put_result_attempts[0], 2)
+        self.assertEqual(self.client.session.headers.get('X-CSRFToken'), 'fresh_csrf_token')
+
     def test_post_back(self):
         def handler(content):
             return {'result': True}
diff --git a/xqueue_watcher/client.py b/xqueue_watcher/client.py
index fbae997..04fb0ca 100644
--- a/xqueue_watcher/client.py
+++ b/xqueue_watcher/client.py
@@ -83,6 +83,7 @@ def _parse_response(self, response, is_reply=True):
     def _request(self, method, uri, **kwargs):
         url = self.xqueue_server + uri
         r = None
+        reauthenticated = False
         while not r:
             try:
                 r = self.session.request(
@@ -102,14 +103,22 @@ def _request(self, method, uri, **kwargs):
             # Django can issue both a 302 to the login page and a
             # 301 if the original URL did not have a trailing / and
             # APPEND_SLASH is true in XQueue deployment, which is the default.
-            elif r.status_code in (301, 302):
+            # DRF returns 401/403 directly when the session is missing or expired.
+            elif r.status_code in (301, 302, 401, 403):
+                if reauthenticated:
+                    # Already re-authenticated once; give up to avoid a login storm.
+                    message = "Received {} after re-authentication, calling {}.".format(
+                        r.status_code, url)
+                    log.error(message)
+                    return (False, message)
+                reauthenticated = True
                 if self._login():
                     r = None
                 else:
                     return (False, "Could not log in")
             else:
-                message = "Received un expected response status code, {}, calling {}.".format(
-                    r.status_code,url)
+                message = "Received unexpected response status code, {}, calling {}. Response: {}".format(
+                    r.status_code, url, r.content)
                 log.error(message)
                 return (False, message)
 
@@ -118,13 +127,62 @@ def _login(self):
             return True
         url = self.xqueue_server + '/xqueue/login/'
         log.debug("Trying to login to %s with user: %s", url, self.username)
-        response = self.session.request('post', url, auth=self.http_basic_auth, verify=_VERIFY_TLS, data={
-            'username': self.username,
-            'password': self.password,
-            })
+        # Clear any stale session/CSRF state so the GET arrives as an anonymous
+        # request.  A stale session cookie causes DRF to return 403 on the GET,
+        # preventing us from obtaining a fresh CSRF cookie.
+        self.session.cookies.clear()
+        self.session.headers.pop('X-CSRFToken', None)
+        # GET the login page so Django sets the csrftoken cookie before we POST.
+        # edx-submissions exposes GET /xqueue/login/ for this purpose
+        # (openedx/edx-submissions#352).  Older deployments that only allow POST
+        # will return 405; we log a warning and proceed without a token — the
+        # login POST is AllowAny so it is CSRF-exempt.
+        get_response = self.session.request(
+            'get',
+            url,
+            auth=self.http_basic_auth,
+            timeout=self.requests_timeout,
+            verify=_VERIFY_TLS,
+        )
+        if get_response.status_code != 200:
+            log.debug(
+                "Login CSRF prefetch returned %d from %s; "
+                "proceeding without CSRF token (older server?)",
+                get_response.status_code, url,
+            )
+        csrf_token = (
+            self.session.cookies.get('csrftoken')
+            or self.session.cookies.get('edx-csrftoken')
+        )
+        login_headers = {'Referer': url}
+        if csrf_token:
+            login_headers['X-CSRFToken'] = csrf_token
+        response = self.session.request(
+            'post',
+            url,
+            auth=self.http_basic_auth,
+            timeout=self.requests_timeout,
+            verify=_VERIFY_TLS,
+            headers=login_headers,
+            data={
+                'username': self.username,
+                'password': self.password,
+            },
+        )
         if response.status_code != 200:
             log.error('Log in error %s %s', response.status_code, response.content)
             return False
+        # Persist the CSRF token and Referer in the session so every subsequent
+        # mutating request (put_result POST) automatically includes them.
+        # Django 4+ rejects HTTPS POST requests that carry no Referer or Origin
+        # header even when the CSRF token itself is correct.
+        csrf_token = (
+            self.session.cookies.get('csrftoken')
+            or self.session.cookies.get('edx-csrftoken')
+        )
+        self.session.headers.update({'Referer': self.xqueue_server})
+        if csrf_token:
+            self.session.headers.update({'X-CSRFToken': csrf_token})
         msg = response.json()
         log.debug("login response from %r: %r", url, msg)
         return msg['return_code'] == 0