diff --git a/gateway/run.py b/gateway/run.py
index 59b172af..ea9f2a28 100644
--- a/gateway/run.py
+++ b/gateway/run.py
@@ -2122,23 +2122,41 @@ class GatewayRunner:
             error_detail = str(e)[:300] if str(e) else "no details available"
             status_hint = ""
             status_code = getattr(e, "status_code", None)
+            _hist_len = len(history) if 'history' in locals() else 0
             if status_code == 401:
                 status_hint = " Check your API key or run `claude /login` to refresh OAuth credentials."
             elif status_code == 429:
-                status_hint = " You are being rate-limited. Please wait a moment and try again."
+                # Check if this is a plan usage limit (resets on a schedule) vs a transient rate limit
+                _err_body = getattr(e, "response", None)
+                _err_json = {}
+                try:
+                    if _err_body is not None:
+                        _err_json = _err_body.json().get("error", {})
+                except Exception:
+                    pass
+                if _err_json.get("type") == "usage_limit_reached":
+                    _resets_in = _err_json.get("resets_in_seconds")
+                    if _resets_in and _resets_in > 0:
+                        import math
+                        _hours = math.ceil(_resets_in / 3600)
+                        status_hint = f" Your plan's usage limit has been reached. It resets in ~{_hours}h."
+                    else:
+                        status_hint = " Your plan's usage limit has been reached. Please wait until it resets."
+                else:
+                    status_hint = " You are being rate-limited. Please wait a moment and try again."
             elif status_code == 529:
                 status_hint = " The API is temporarily overloaded. Please try again shortly."
-            elif status_code == 400:
-                # 400 with a large session is almost always a context overflow.
-                # Give specific guidance instead of a generic error. (#1630)
-                _hist_len = len(history) if 'history' in locals() else 0
+            elif status_code in (400, 500):
+                # 400 with a large session is context overflow.
+                # 500 with a large session often means the payload is too large
+                # for the API to process — treat it the same way.
                 if _hist_len > 50:
                     return (
                         "⚠️ Session too large for the model's context window.\n"
                         "Use /compact to compress the conversation, or "
                         "/reset to start fresh."
                     )
-                else:
+                elif status_code == 400:
                     status_hint = " The request was rejected by the API."
             return (
                 f"Sorry, I encountered an error ({error_type}).\n"