diff --git a/src/murfey/client/update.py b/src/murfey/client/update.py
index d000b430e..49570bd1b 100644
--- a/src/murfey/client/update.py
+++ b/src/murfey/client/update.py
@@ -15,8 +15,9 @@ def check(api_base: ParseResult, install: bool = True, force: bool = False):
     If the version number is outside the allowed range then this can trigger
     an update on the client, and in that case will terminate the process.
     """
+    proxy_path = api_base.path.rstrip("/")
     version_check_url = api_base._replace(
-        path="/version", query=f"client_version={murfey.__version__}"
+        path=f"{proxy_path}/version/", query=f"client_version={murfey.__version__}"
     )
     server_reply = requests.get(version_check_url.geturl())
     if server_reply.status_code != 200:
@@ -59,6 +60,7 @@ def install_murfey(api_base: ParseResult, version: str) -> bool:
     Return 'true' on success and 'false' on error."""
 
     assert api_base.hostname is not None
+    proxy_path = api_base.path.rstrip("/")
     result = subprocess.run(
         [
             sys.executable,
@@ -67,7 +69,7 @@ def install_murfey(api_base: ParseResult, version: str) -> bool:
             "--trusted-host",
             api_base.hostname,
             "-i",
-            api_base._replace(path="/pypi", query="").geturl(),
+            api_base._replace(path=f"{proxy_path}/pypi", query="").geturl(),
             f"murfey[client]=={version}",
         ]
     )
diff --git a/src/murfey/client/websocket.py b/src/murfey/client/websocket.py
index 956800218..d693f14b9 100644
--- a/src/murfey/client/websocket.py
+++ b/src/murfey/client/websocket.py
@@ -25,16 +25,24 @@ def __init__(
         self.id = uuid.uuid4() if id is None else id
         log.info(f"Opening websocket connection for Client {self.id}")
         websocket.enableTrace(True)
-        url = urllib.parse.urlparse(server)._replace(scheme="ws", path="")
+
+        # Parse server URL and get proxy path used, if any
+        url = urllib.parse.urlparse(server)._replace(scheme="ws")
+        proxy_path = url.path.rstrip("/")
+
         self._address = url.geturl()
         self._alive = True
         self._ready = False
         self._send_queue: queue.Queue[Optional[str]] = queue.Queue()
         self._receive_queue: queue.Queue[Optional[str]] = queue.Queue()
+
+        # Construct the websocket URL
+        # Prepend the proxy path to the new URL path
+        # It will evaluate to "" if nothing's there, and starts with "/" if present
         ws_url = (
-            url._replace(path=f"/ws/test/{self.id}").geturl()
+            url._replace(path=f"{proxy_path}/ws/test/{self.id}").geturl()
             if register_client
-            else url._replace(path=f"/ws/connect/{self.id}").geturl()
+            else url._replace(path=f"{proxy_path}/ws/connect/{self.id}").geturl()
         )
         self._ws = websocket.WebSocketApp(
             ws_url,