diff --git a/synapse/handlers/oidc_handler.py b/synapse/handlers/oidc_handler.py
index 3adc75fa4ab4..8a5c7a4df903 100644
--- a/synapse/handlers/oidc_handler.py
+++ b/synapse/handlers/oidc_handler.py
@@ -161,13 +161,9 @@ async def handle_oidc_callback(self, request: SynapseRequest) -> None:
         # Remove the cookie. There is a good chance that if the callback failed
         # once, it will fail next time and the code will already be exchanged.
         # Removing it early avoids spamming the provider with token requests.
-        request.addCookie(
-            SESSION_COOKIE_NAME,
-            b"",
-            path="/_synapse/oidc",
-            expires="Thu, Jan 01 1970 00:00:00 UTC",
-            httpOnly=True,
-            sameSite="lax",
+        request.cookies.append(
+            b"%s=; Path=/_synapse/client/oidc; Expires=Thu, Jan 01 1970 00:00:00 UTC; "
+            b"HttpOnly; SameSite=None; Secure" % (SESSION_COOKIE_NAME,)
         )
 
         # Check for the state query parameter
@@ -693,13 +689,17 @@ async def handle_redirect_request(
                 ui_auth_session_id=ui_auth_session_id,
             ),
         )
-        request.addCookie(
-            SESSION_COOKIE_NAME,
-            cookie,
-            path="/_synapse/client/oidc",
-            max_age="3600",
-            httpOnly=True,
-            sameSite="lax",
+
+        # we set SameSite=None to ensure that the cookie is included in any POST
+        # requests to our callback (as is used with `response_mode=form_post`).
+        #
+        # Secure is necessary for SameSite=None
+        #
+        # we have to build the cookie by hand rather than calling request.addCookie
+        # to work around https://twistedmatrix.com/trac/ticket/10088
+        request.cookies.append(
+            b"%s=%s; Path=/_synapse/client/oidc; Max-Age=3600; HttpOnly; "
+            b"SameSite=None; Secure" % (SESSION_COOKIE_NAME, cookie.encode("utf-8"))
         )
 
         metadata = await self.load_metadata()
diff --git a/tests/handlers/test_oidc.py b/tests/handlers/test_oidc.py
index ad20400b1dbc..a09f0a40b994 100644
--- a/tests/handlers/test_oidc.py
+++ b/tests/handlers/test_oidc.py
@@ -308,7 +308,9 @@ def test_skip_verification(self):
 
     def test_redirect_request(self):
         """The redirect request has the right arguments & generates a valid session cookie."""
-        req = Mock(spec=["addCookie"])
+        req = Mock(spec=["cookies"])
+        req.cookies = []
+
         url = self.get_success(
             self.provider.handle_redirect_request(req, b"http://client/redirect")
         )
@@ -328,18 +330,15 @@ def test_redirect_request(self):
         self.assertEqual(len(params["nonce"]), 1)
 
         # Check what is in the cookie
-        # note: python3.5 mock does not have the .called_once() method
-        calls = req.addCookie.call_args_list
-        self.assertEqual(len(calls), 1)  # called once
-        # For some reason, call.args does not work with python3.5
-        args = calls[0][0]
-        kwargs = calls[0][1]
+        self.assertEqual(len(req.cookies), 1)  # one cookie
+        cookie_header = req.cookies[0]
 
         # The cookie name and path don't really matter, just that it has to be coherent
         # between the callback & redirect handlers.
-        self.assertEqual(args[0], b"oidc_session")
-        self.assertEqual(kwargs["path"], "/_synapse/client/oidc")
-        cookie = args[1]
+        parts = [p.strip() for p in cookie_header.split(b";")]
+        self.assertIn(b"Path=/_synapse/client/oidc", parts)
+        name, cookie = parts[0].split(b"=")
+        self.assertEqual(name, b"oidc_session")
 
         macaroon = pymacaroons.Macaroon.deserialize(cookie)
         state = self.handler._token_generator._get_value_from_macaroon(
@@ -470,7 +469,7 @@ def test_callback(self):
 
     def test_callback_session(self):
         """The callback verifies the session presence and validity"""
-        request = Mock(spec=["args", "getCookie", "addCookie"])
+        request = Mock(spec=["args", "getCookie", "cookies"])
 
         # Missing cookie
         request.args = {}
@@ -910,13 +909,14 @@ def _build_callback_request(
         spec=[
             "args",
             "getCookie",
-            "addCookie",
+            "cookies",
             "requestHeaders",
             "getClientIP",
             "getHeader",
         ]
     )
 
+    request.cookies = []
     request.getCookie.return_value = session
     request.args = {}
     request.args[b"code"] = [code.encode("utf-8")]