diff --git a/py/lora_manager.py b/py/lora_manager.py
index 1f66ddb4..88029eb8 100644
--- a/py/lora_manager.py
+++ b/py/lora_manager.py
@@ -33,6 +33,7 @@ from .utils.example_images_migration import ExampleImagesMigration
 from .services.websocket_manager import ws_manager
 from .services.example_images_cleanup_service import ExampleImagesCleanupService
 from .middleware.csp_middleware import relax_csp_for_remote_media
+from .middleware.error_middleware import api_json_error
 
 logger = logging.getLogger(__name__)
 
@@ -76,6 +77,11 @@ class LoraManager:
         """Initialize and register all routes using the new refactored architecture"""
         app = PromptServer.instance.app
 
+        # Register JSON error middleware for /api/* routes as the outermost
+        # middleware so it catches errors from all other middlewares.
+        if api_json_error not in app.middlewares:
+            app.middlewares.insert(0, api_json_error)
+
         if relax_csp_for_remote_media not in app.middlewares:
             # Ensure CSP relaxer executes after ComfyUI's block_external_middleware so it can
             # see and extend the restrictive header instead of being overwritten by it.
diff --git a/py/middleware/error_middleware.py b/py/middleware/error_middleware.py
new file mode 100644
index 00000000..cea0332f
--- /dev/null
+++ b/py/middleware/error_middleware.py
@@ -0,0 +1,71 @@
+"""JSON error middleware for API routes.
+
+Ensures all responses to /api/* requests return valid JSON that the
+browser-extension frontend can JSON.parse() without crashing, even when
+the route does not exist (404) or the handler raises an exception (500).
+
+Extension consumers call response.json() unconditionally — an HTML error
+page causes ``SyntaxError: unexpected end of data`` that leaks into the
+popup UI as a toast notification.
+"""
+
+from __future__ import annotations
+
+import logging
+from typing import Awaitable, Callable
+
+from aiohttp import web
+
+logger = logging.getLogger(__name__)
+
+
+@web.middleware
+async def api_json_error(
+    request: web.Request,
+    handler: Callable[[web.Request], Awaitable[web.Response]],
+) -> web.Response:
+    """Return JSON ``{"success": false, "error": "..."}`` for API errors.
+
+    Only intercepts paths starting with ``/api/`` — all other routes
+    (frontend pages, static files, WebSocket upgrades) pass through
+    unchanged.
+    """
+    if not request.path.startswith("/api/"):
+        return await handler(request)
+
+    try:
+        response = await handler(request)
+        return response
+    except web.HTTPException as exc:
+        # Let redirects (301, 302, 307, 308) propagate — they are not errors.
+        if exc.status < 400:
+            raise
+
+        logger.warning(
+            "API %s %s returned HTTP %d: %s",
+            request.method,
+            request.path,
+            exc.status,
+            exc.reason,
+        )
+
+        return web.json_response(
+            {"success": False, "error": f"{exc.status}: {exc.reason}"},
+            status=exc.status,
+        )
+    except Exception as exc:
+        logger.error(
+            "API %s %s raised unhandled exception: %s",
+            request.method,
+            request.path,
+            exc,
+            exc_info=True,
+        )
+
+        return web.json_response(
+            {
+                "success": False,
+                "error": f"500: Internal Server Error ({type(exc).__name__})",
+            },
+            status=500,
+        )
diff --git a/standalone.py b/standalone.py
index c03645df..298d057f 100644
--- a/standalone.py
+++ b/standalone.py
@@ -2,6 +2,7 @@ import os
 import sys
 import json
 from py.middleware.cache_middleware import cache_control
+from py.middleware.error_middleware import api_json_error
 from py.utils.settings_paths import ensure_settings_file
 
 # Set environment variable to indicate standalone mode
@@ -157,7 +158,7 @@ class StandaloneServer:
     def __init__(self):
         self.app = web.Application(
             logger=logger,
-            middlewares=[cache_control],
+            middlewares=[api_json_error, cache_control],
             client_max_size=256 * 1024 * 1024,
             handler_args={
                 "max_field_size": HEADER_SIZE_LIMIT,