diff --git a/backend/open_webui/routers/terminals.py b/backend/open_webui/routers/terminals.py
index 6b5cd6e1d3..ef6cbd01e2 100644
--- a/backend/open_webui/routers/terminals.py
+++ b/backend/open_webui/routers/terminals.py
@@ -107,6 +107,8 @@ PROXY_METHODS = ['GET', 'POST', 'PUT', 'PATCH', 'DELETE', 'HEAD', 'OPTIONS']
 
 
 @router.api_route('/{server_id}/{path:path}', methods=PROXY_METHODS)
+# Must stay the lower decorator so it registers before the catch-all, which would swallow chat paths.
+@router.api_route('/{server_id}/chats/{chat_id}/{path:path}', methods=PROXY_METHODS)
 async def proxy_terminal(
     server_id: str,
     path: str,
@@ -151,7 +153,7 @@ async def proxy_terminal(
 
     headers = {'X-User-Id': user.id}
     # Forward per-session cwd tracking header
-    session_id = request.headers.get('x-session-id')
+    session_id = request.path_params.get('chat_id') or request.headers.get('x-session-id')
     if session_id:
         headers['X-Session-Id'] = session_id
         if not terminal_context_available(connection, 'chat'):
diff --git a/src/lib/components/chat/FileNav.svelte b/src/lib/components/chat/FileNav.svelte
index e2d9aed0af..08085adb7c 100644
--- a/src/lib/components/chat/FileNav.svelte
+++ b/src/lib/components/chat/FileNav.svelte
@@ -355,6 +355,11 @@
 	let selectedTerminal: { url: string; key: string } | null = null;
 	let terminalChatContextPending = false;
 	let terminalChatContextHidden = false;
+	let scopedChatId: string | null = null;
+	$: portBaseUrl =
+		selectedTerminal && scopedChatId
+			? `${selectedTerminal.url}/chats/${encodeURIComponent(scopedChatId)}`
+			: (selectedTerminal?.url ?? '');
 
 	const chatContext = (terminal: any) => terminal?.contexts?.chat ?? {};
 
@@ -364,6 +369,7 @@
 			: ($terminalServers?.[0] ?? null);
 		const chatConfig = chatContext(systemTerminal);
 		const chatScoped = !!systemTerminal && chatConfig?.context_id === 'chat_id';
+		scopedChatId = chatScoped ? chatId : null;
 		terminalChatContextHidden =
 			!!systemTerminal && (chatConfig === false || (chatScoped && isTemporaryChatId(chatId)));
 		terminalChatContextPending = chatScoped && !terminalChatContextHidden && !isSavedChatId(chatId);
@@ -1824,7 +1830,7 @@
 				/>
 			{:else if previewPort !== null}
 				<PortPreview
-					baseUrl={selectedTerminal?.url ?? ''}
+					baseUrl={portBaseUrl}
 					port={previewPort}
 					overlay={overlay || isDraggingHandle}
 					onClose={() => {
@@ -2099,7 +2105,7 @@
 		{#if selectedTerminal && !selectedFile && previewPort === null && !isSearching}
 			<div class="shrink-0 border-t border-gray-50 dark:border-gray-850/30">
 				<PortList
-					baseUrl={selectedTerminal.url}
+					baseUrl={portBaseUrl}
 					apiKey={selectedTerminal.key}
 					on:previewPort={(e) => {
 						selectedFile = null;