diff --git a/changelog.d/9726.bugfix b/changelog.d/9726.bugfix
new file mode 100644
index 000000000000..4ba0b24327cb
--- /dev/null
+++ b/changelog.d/9726.bugfix
@@ -0,0 +1 @@
+Fixes the OIDC SSO flow when using a `public_baseurl` value including a non-root URL path.
\ No newline at end of file
diff --git a/synapse/config/server.py b/synapse/config/server.py
index 02b86b11a5ee..21ca7b33e38d 100644
--- a/synapse/config/server.py
+++ b/synapse/config/server.py
@@ -235,7 +235,11 @@ def read_config(self, config, **kwargs):
         self.print_pidfile = config.get("print_pidfile")
         self.user_agent_suffix = config.get("user_agent_suffix")
         self.use_frozen_dicts = config.get("use_frozen_dicts", False)
+
         self.public_baseurl = config.get("public_baseurl")
+        if self.public_baseurl is not None:
+            if self.public_baseurl[-1] != "/":
+                self.public_baseurl += "/"
 
         # Whether to enable user presence.
         presence_config = config.get("presence") or {}
@@ -407,10 +411,6 @@ def read_config(self, config, **kwargs):
             config_path=("federation_ip_range_blacklist",),
         )
 
-        if self.public_baseurl is not None:
-            if self.public_baseurl[-1] != "/":
-                self.public_baseurl += "/"
-
         # (undocumented) option for torturing the worker-mode replication a bit,
         # for testing. The value defines the number of milliseconds to pause before
         # sending out any replication updates.
diff --git a/synapse/handlers/oidc.py b/synapse/handlers/oidc.py
index 1c4a43be0a81..ee6e41c0e4d9 100644
--- a/synapse/handlers/oidc.py
+++ b/synapse/handlers/oidc.py
@@ -15,7 +15,7 @@
 import inspect
 import logging
 from typing import TYPE_CHECKING, Dict, Generic, List, Optional, TypeVar, Union
-from urllib.parse import urlencode
+from urllib.parse import urlencode, urlparse
 
 import attr
 import pymacaroons
@@ -68,8 +68,8 @@
 #
 # Here we have the names of the cookies, and the options we use to set them.
 _SESSION_COOKIES = [
-    (b"oidc_session", b"Path=/_synapse/client/oidc; HttpOnly; Secure; SameSite=None"),
-    (b"oidc_session_no_samesite", b"Path=/_synapse/client/oidc; HttpOnly"),
+    (b"oidc_session", b"HttpOnly; Secure; SameSite=None"),
+    (b"oidc_session_no_samesite", b"HttpOnly"),
 ]
 
 #: A token exchanged from the token endpoint, as per RFC6749 sec 5.1. and
@@ -279,6 +279,13 @@ def __init__(
         self._config = provider
         self._callback_url = hs.config.oidc_callback_url  # type: str
 
+        # Calculate the prefix for OIDC callback paths based on the public_baseurl.
+        # We'll insert this into the Path= parameter of any session cookies we set.
+        public_baseurl_path = urlparse(hs.config.server.public_baseurl).path
+        self._callback_path_prefix = (
+            public_baseurl_path.encode("utf-8") + b"_synapse/client/oidc"
+        )
+
         self._oidc_attribute_requirements = provider.attribute_requirements
         self._scopes = provider.scopes
         self._user_profile_method = provider.user_profile_method
@@ -779,8 +786,13 @@ async def handle_redirect_request(
 
         for cookie_name, options in _SESSION_COOKIES:
             request.cookies.append(
-                b"%s=%s; Max-Age=3600; %s"
-                % (cookie_name, cookie.encode("utf-8"), options)
+                b"%s=%s; Max-Age=3600; Path=%s; %s"
+                % (
+                    cookie_name,
+                    cookie.encode("utf-8"),
+                    self._callback_path_prefix,
+                    options,
+                )
             )
 
         metadata = await self.load_metadata()