diff --git a/rust-runtime/aws-smithy-http-server-python/src/middleware/error.rs b/rust-runtime/aws-smithy-http-server-python/src/middleware/error.rs
index 69289865a9a..832fd5bae13 100644
--- a/rust-runtime/aws-smithy-http-server-python/src/middleware/error.rs
+++ b/rust-runtime/aws-smithy-http-server-python/src/middleware/error.rs
@@ -1,23 +1,20 @@
-use std::error::Error;
-use std::fmt;
-
 use pyo3::{exceptions::PyRuntimeError, PyErr};
+use thiserror::Error;
 
-#[derive(Debug)]
+/// Possible middleware errors that might arise.
+#[derive(Error, Debug)]
 pub enum PyMiddlewareError {
-    ResponseAlreadyGone,
+    /// Returned when `next` is called multiple times.
+    #[error("next already called")]
+    NextAlreadyCalled,
+    /// Returned when request is accessed after `next` is called.
+    #[error("request is gone")]
+    RequestGone,
+    /// Returned when response is called after it is returned.
+    #[error("response is gone")]
+    ResponseGone,
 }
 
-impl fmt::Display for PyMiddlewareError {
-    fn fmt(&self, f: &mut fmt::Formatter) -> fmt::Result {
-        match *self {
-            Self::ResponseAlreadyGone => write!(f, "response is already consumed"),
-        }
-    }
-}
-
-impl Error for PyMiddlewareError {}
-
 impl From<PyMiddlewareError> for PyErr {
     fn from(err: PyMiddlewareError) -> PyErr {
         PyRuntimeError::new_err(err.to_string())
diff --git a/rust-runtime/aws-smithy-http-server-python/src/middleware/handler.rs b/rust-runtime/aws-smithy-http-server-python/src/middleware/handler.rs
index 22bcfedbcd6..6a14205c0cf 100644
--- a/rust-runtime/aws-smithy-http-server-python/src/middleware/handler.rs
+++ b/rust-runtime/aws-smithy-http-server-python/src/middleware/handler.rs
@@ -36,10 +36,10 @@ impl PyNext {
         let req = py_req
             .borrow_mut(py)
             .take_inner()
-            .ok_or_else(|| PyRuntimeError::new_err("already called"))?;
+            .ok_or(PyMiddlewareError::RequestGone)?;
         let mut inner = self
             .take_inner()
-            .ok_or_else(|| PyRuntimeError::new_err("already called"))?;
+            .ok_or(PyMiddlewareError::NextAlreadyCalled)?;
         pyo3_asyncio::tokio::future_into_py(py, async move {
             let res = inner
                 .call(req)
@@ -105,6 +105,6 @@ impl PyMiddlewareHandler {
             Ok::<_, PyErr>(py_res.take_inner())
         })?;
 
-        response.ok_or_else(|| PyMiddlewareError::ResponseAlreadyGone.into())
+        response.ok_or_else(|| PyMiddlewareError::ResponseGone.into())
     }
 }
diff --git a/rust-runtime/aws-smithy-http-server-python/src/middleware/pytests/layer.rs b/rust-runtime/aws-smithy-http-server-python/src/middleware/pytests/layer.rs
index 9a23844282e..982cc3e067e 100644
--- a/rust-runtime/aws-smithy-http-server-python/src/middleware/pytests/layer.rs
+++ b/rust-runtime/aws-smithy-http-server-python/src/middleware/pytests/layer.rs
@@ -238,3 +238,57 @@ def second_middleware(request, next):
     assert_eq!(body, "hello client from Python second middleware");
     Ok(())
 }
+
+#[pyo3_asyncio::tokio::test]
+async fn fails_if_req_is_used_after_calling_next() -> PyResult<()> {
+    let locals = Python::with_gil(|py| {
+        Ok::<_, PyErr>(TaskLocals::new(pyo3_asyncio::tokio::get_current_loop(py)?))
+    })?;
+    let handler = Python::with_gil(|py| {
+        let locals = PyDict::new(py);
+        py.run(
+            r#"
+async def middleware(request, next):
+    uri = request.uri
+    response = await next(request)
+    uri = request.uri # <- fails
+    return response
+"#,
+            None,
+            Some(locals),
+        )?;
+        let handler = locals.get_item("middleware").unwrap().into();
+        Ok::<_, PyErr>(PyMiddlewareHandler::new(py, handler)?)
+    })?;
+
+    let layer = PyMiddlewareLayer::<RestJson1>::new(handler, locals);
+    let (mut service, mut handle) = mock::spawn_with(|svc| {
+        let svc = svc.map_err(|err| panic!("service failed: {err}"));
+        let svc = layer.layer(svc);
+        svc
+    });
+    assert_ready_ok!(service.poll_ready());
+
+    let th = tokio::spawn(async move {
+        let (req, send_response) = handle.next_request().await.unwrap();
+        let req_body = hyper::body::to_bytes(req.into_body()).await.unwrap();
+        assert_eq!(req_body, "hello server");
+        send_response.send_response(
+            Response::builder()
+                .body(to_boxed("hello client"))
+                .expect("could not create response"),
+        );
+    });
+
+    let request = Request::builder()
+        .body(Body::from("hello server"))
+        .expect("could not create request");
+    let response = service.call(request);
+
+    let response = response.await.unwrap();
+    assert_eq!(response.status(), StatusCode::INTERNAL_SERVER_ERROR);
+    let body = hyper::body::to_bytes(response.into_body()).await.unwrap();
+    assert_eq!(body, r#"{"message":"RuntimeError: request is gone"}"#);
+    th.await.unwrap();
+    Ok(())
+}
diff --git a/rust-runtime/aws-smithy-http-server-python/src/util.rs b/rust-runtime/aws-smithy-http-server-python/src/util.rs
index 118c9cac58b..c2dd5bf675a 100644
--- a/rust-runtime/aws-smithy-http-server-python/src/util.rs
+++ b/rust-runtime/aws-smithy-http-server-python/src/util.rs
@@ -40,6 +40,8 @@ mod tests {
 
     #[test]
     fn function_metadata() -> PyResult<()> {
+        pyo3::prepare_freethreaded_python();
+
         Python::with_gil(|py| {
             let module = PyModule::from_code(
                 py,