diff --git a/aws_lambda_powertools/event_handler/api_gateway.py b/aws_lambda_powertools/event_handler/api_gateway.py
index 25b34613f44..4fb4a6ce258 100644
--- a/aws_lambda_powertools/event_handler/api_gateway.py
+++ b/aws_lambda_powertools/event_handler/api_gateway.py
@@ -2560,7 +2560,10 @@ def resolve(self, event: Mapping[str, Any], context: LambdaContext) -> dict[str,
         BaseRouter.current_event = self._to_proxy_event(cast(dict, event))
         BaseRouter.lambda_context = context
 
-        response = self._build_response(self._resolve())
+        try:
+            response = self._build_response(self._resolve())
+        finally:
+            self.clear_context()
 
         # Debug print Processed Middlewares
         if self._debug:
@@ -2569,8 +2572,6 @@ def resolve(self, event: Mapping[str, Any], context: LambdaContext) -> dict[str,
             print("\n".join(self.processed_stack_frames))
             print("======================")
 
-        self.clear_context()
-
         return response
 
     async def resolve_async(self, event: Mapping[str, Any], context: LambdaContext) -> dict[str, Any]:
@@ -2621,7 +2622,10 @@ def lambda_handler(event, context):
         BaseRouter.current_event = self._to_proxy_event(cast(dict, event))
         BaseRouter.lambda_context = context
 
-        response = self._build_response(await self._resolve_async())
+        try:
+            response = self._build_response(await self._resolve_async())
+        finally:
+            self.clear_context()
 
         if self._debug:
             print("\nProcessed Middlewares:")
@@ -2629,8 +2633,6 @@ def lambda_handler(event, context):
             print("\n".join(self.processed_stack_frames))
             print("======================")
 
-        self.clear_context()
-
         return response
 
     def _build_response(self, response_builder: ResponseBuilder) -> dict[str, Any]:
@@ -3401,20 +3403,16 @@ def _build_response(self, response_builder: ResponseBuilder) -> dict[str, Any]:
         try:
             self._validate_response_size(response)
         except ResponseSizeExceededError as exc:
-            try:
-                # Resolved responses retain their route, including not-found and preflight responses.
-                handled_response = self._call_exception_handler(exc, cast(Route, response_builder.route))
-                if handled_response is None:
-                    raise
-
-                handled_response.response = cast(Response, self._to_response(handled_response.response))
-                response = super()._build_response(handled_response)
-                # Validate once more without invoking an exception handler recursively.
-                self._validate_response_size(response)
-            except Exception:
-                self.clear_context()
+            # Resolved responses retain their route, including not-found and preflight responses.
+            handled_response = self._call_exception_handler(exc, cast(Route, response_builder.route))
+            if handled_response is None:
                 raise
 
+            handled_response.response = cast(Response, self._to_response(handled_response.response))
+            response = super()._build_response(handled_response)
+            # Validate once more without invoking an exception handler recursively.
+            self._validate_response_size(response)
+
         return response
 
     @staticmethod
diff --git a/tests/functional/auth_alpha/jwt/integrations/test_middleware.py b/tests/functional/auth_alpha/jwt/integrations/test_middleware.py
index 97639182528..bde43f6887b 100644
--- a/tests/functional/auth_alpha/jwt/integrations/test_middleware.py
+++ b/tests/functional/auth_alpha/jwt/integrations/test_middleware.py
@@ -84,8 +84,7 @@ def public():
     event["headers"] = {"authorization": "Bearer " + issue_token()}
     with pytest.raises(RuntimeError, match="handler failed"):
         app.resolve(event, {})
-    assert "claims" not in app.context
-    assert app.context["application_value"] == "preserved"
+    assert app.context == {}
 
     event["headers"] = {}
     public_event = copy.deepcopy(event)
diff --git a/tests/functional/event_handler/required_dependencies/test_api_gateway.py b/tests/functional/event_handler/required_dependencies/test_api_gateway.py
index dec2e6d3b2b..65d1a50082d 100644
--- a/tests/functional/event_handler/required_dependencies/test_api_gateway.py
+++ b/tests/functional/event_handler/required_dependencies/test_api_gateway.py
@@ -1892,6 +1892,23 @@ def my_path():
     assert app.context == {}
 
 
+def test_route_context_is_cleared_when_handler_raises():
+    # GIVEN a route that raises an exception without a registered exception handler
+    app = APIGatewayRestResolver()
+    app.append_context(is_admin=True)
+
+    @app.get("/my/path")
+    def my_path():
+        raise ValueError("boom")
+
+    # WHEN event resolution kicks in
+    with pytest.raises(ValueError, match="boom"):
+        app.resolve(LOAD_GW_EVENT, {})
+
+    # THEN context should be cleared even though the route raised
+    assert app.context == {}
+
+
 def test_router_has_access_to_app_context(json_dump):
     # GIVEN a Router with registered routes
     app = ApiGatewayResolver()
diff --git a/tests/functional/event_handler/required_dependencies/test_request.py b/tests/functional/event_handler/required_dependencies/test_request.py
index b00ae6659ba..e1147f3805b 100644
--- a/tests/functional/event_handler/required_dependencies/test_request.py
+++ b/tests/functional/event_handler/required_dependencies/test_request.py
@@ -321,6 +321,24 @@ def handler(counter_id: str, request: Request):
     assert call_count == 3
 
 
+def test_request_is_not_reused_after_unhandled_exception():
+    """A handler raising must not leave its Request cached for the next invocation."""
+    app = APIGatewayRestResolver()
+    received: list[Request] = []
+
+    @app.get("/counters/<counter_id>")
+    def handler(counter_id: str, request: Request):
+        received.append(request)
+        raise ValueError(counter_id)
+
+    for i in range(2):
+        event = _make_rest_event(f"/counters/{i}", path_parameters={"counter_id": str(i)})
+        with pytest.raises(ValueError):
+            app(event, {})
+
+    assert [req.path_parameters for req in received] == [{"counter_id": "0"}, {"counter_id": "1"}]
+
+
 # ---------------------------------------------------------------------------
 # RuntimeError when accessed outside of request resolution
 # ---------------------------------------------------------------------------
diff --git a/tests/functional/event_handler/required_dependencies/test_resolve_async.py b/tests/functional/event_handler/required_dependencies/test_resolve_async.py
index e9b12ce2a2d..d15895f6a6c 100644
--- a/tests/functional/event_handler/required_dependencies/test_resolve_async.py
+++ b/tests/functional/event_handler/required_dependencies/test_resolve_async.py
@@ -456,6 +456,22 @@ async def get_lambda():
         # THEN the context is cleared after resolution
         assert app.context == {}
 
+    def test_resolve_async_clears_context_when_handler_raises(self, public_resolver_and_event):
+        # GIVEN an async handler that raises without a registered exception handler
+        app, event, path = public_resolver_and_event
+
+        @app.get(path)
+        async def get_lambda():
+            app.append_context(custom_key="value")
+            raise ValueError("boom")
+
+        # WHEN calling resolve_async
+        with pytest.raises(ValueError, match="boom"):
+            asyncio.run(app.resolve_async(event, MockLambdaContext()))
+
+        # THEN the context is still cleared
+        assert app.context == {}
+
     def test_resolve_async_not_found(self, public_resolver_and_event):
         # GIVEN no matching route
         app, event, _path = public_resolver_and_event