diff --git a/rust-runtime/aws-smithy-http-server/src/request/connect_info.rs b/rust-runtime/aws-smithy-http-server/src/request/connect_info.rs
index 71b744ef5b..ce6b6f1600 100644
--- a/rust-runtime/aws-smithy-http-server/src/request/connect_info.rs
+++ b/rust-runtime/aws-smithy-http-server/src/request/connect_info.rs
@@ -12,14 +12,31 @@
 //! and [`ConnectInfo`] with a service builder.
 
 use http::request::Parts;
+use thiserror::Error;
 
-use crate::Extension;
+use crate::{body::BoxBody, response::IntoResponse};
 
-use super::FromParts;
+use super::{internal_server_error, FromParts};
+
+/// The [`ConnectInfo`] was not found in the [`http::Request`] extensions.
+///
+/// Use [`IntoMakeServiceWithConnectInfo`](crate::routing::IntoMakeServiceWithConnectInfo) to ensure it's present.
+#[non_exhaustive]
+#[derive(Debug, Error)]
+#[error(
+    "`ConnectInfo` is not present in the `http::Request` extensions - consider using `aws_smithy_http_server::routing::IntoMakeServiceWithConnectInfo`"
+)]
+pub struct MissingConnectInfo;
+
+impl<Protocol> IntoResponse<Protocol> for MissingConnectInfo {
+    fn into_response(self) -> http::Response<BoxBody> {
+        internal_server_error()
+    }
+}
 
 /// Extractor for getting connection information produced by a `Connected`.
 ///
-/// Note this extractor requires the existence of [`Extension<ConnectInfo<T>>`] in the [`http::Extensions`]. This is
+/// Note this extractor requires the existence of [`ConnectInfo<T>`] in the [`http::Extensions`]. This is
 /// automatically inserted by the [`IntoMakeServiceWithConnectInfo`](crate::routing::IntoMakeServiceWithConnectInfo)
 /// middleware, which can be applied using the `into_make_service_with_connect_info` method on your generated service.
 #[derive(Clone, Debug)]
@@ -29,10 +46,9 @@ impl<P, T> FromParts<P> for ConnectInfo<T>
 where
     T: Send + Sync + 'static,
 {
-    type Rejection = <Extension<Self> as FromParts<P>>::Rejection;
+    type Rejection = MissingConnectInfo;
 
     fn from_parts(parts: &mut Parts) -> Result<Self, Self::Rejection> {
-        let Extension(connect_info) = <Extension<Self> as FromParts<P>>::from_parts(parts)?;
-        Ok(connect_info)
+        parts.extensions.remove().ok_or(MissingConnectInfo)
     }
 }
diff --git a/rust-runtime/aws-smithy-http-server/src/request/extension.rs b/rust-runtime/aws-smithy-http-server/src/request/extension.rs
index 7aaf23ff2c..b7f10683eb 100644
--- a/rust-runtime/aws-smithy-http-server/src/request/extension.rs
+++ b/rust-runtime/aws-smithy-http-server/src/request/extension.rs
@@ -50,14 +50,11 @@
 
 use std::ops::Deref;
 
-use http::StatusCode;
 use thiserror::Error;
 
-use crate::{
-    body::{empty, BoxBody},
-    request::FromParts,
-    response::IntoResponse,
-};
+use crate::{body::BoxBody, request::FromParts, response::IntoResponse};
+
+use super::internal_server_error;
 
 /// Generic extension type stored in and extracted from [request extensions].
 ///
@@ -79,15 +76,14 @@ impl<T> Deref for Extension<T> {
 }
 
 /// The extension has not been added to the [`Request`](http::Request) or has been previously removed.
+#[non_exhaustive]
 #[derive(Debug, Error)]
 #[error("the `Extension` is not present in the `http::Request`")]
 pub struct MissingExtension;
 
 impl<Protocol> IntoResponse<Protocol> for MissingExtension {
     fn into_response(self) -> http::Response<BoxBody> {
-        let mut response = http::Response::new(empty());
-        *response.status_mut() = StatusCode::INTERNAL_SERVER_ERROR;
-        response
+        internal_server_error()
     }
 }
 
diff --git a/rust-runtime/aws-smithy-http-server/src/request/lambda.rs b/rust-runtime/aws-smithy-http-server/src/request/lambda.rs
index c78e212726..6088ee8f94 100644
--- a/rust-runtime/aws-smithy-http-server/src/request/lambda.rs
+++ b/rust-runtime/aws-smithy-http-server/src/request/lambda.rs
@@ -12,41 +12,109 @@ pub use lambda_http::{
     aws_lambda_events::apigw::{ApiGatewayProxyRequestContext, ApiGatewayV2httpRequestContext},
     Context,
 };
+use thiserror::Error;
 
-use super::{extension::MissingExtension, FromParts};
-use crate::Extension;
+use super::{internal_server_error, FromParts};
+use crate::{body::BoxBody, response::IntoResponse};
+
+/// The [`Context`] was not found in the [`http::Request`] extensions.
+///
+/// Use [`LambdaHandler`](crate::routing::LambdaHandler) to ensure it's present.
+#[non_exhaustive]
+#[derive(Debug, Error)]
+#[error("`Context` is not present in the `http::Request` extensions - consider using `aws_smithy_http_server::routing::LambdaHandler`")]
+pub struct MissingContext;
+
+impl<Protocol> IntoResponse<Protocol> for MissingContext {
+    fn into_response(self) -> http::Response<BoxBody> {
+        internal_server_error()
+    }
+}
 
 impl<P> FromParts<P> for Context {
-    type Rejection = MissingExtension;
+    type Rejection = MissingContext;
 
     fn from_parts(parts: &mut http::request::Parts) -> Result<Self, Self::Rejection> {
-        let Extension(context) = <Extension<Self> as FromParts<P>>::from_parts(parts)?;
-        Ok(context)
+        parts.extensions.remove().ok_or(MissingContext)
+    }
+}
+
+#[derive(Debug, Error)]
+enum MissingGatewayContextTypeV1 {
+    #[error("`RequestContext` is not present in the `http::Request` extensions - consider using `aws_smithy_http_server::routing::LambdaHandler`")]
+    MissingRequestContext,
+    #[error("`RequestContext::ApiGatewayV2` is present in the `http::Request` extensions - consider using the `aws_smithy_http_server::request::lambda::ApiGatewayV2httpRequestContext` extractor")]
+    VersionMismatch,
+}
+
+/// The [`RequestContext::ApiGatewayV1`] was not found in the [`http::Request`] extensions.
+///
+/// Use [`LambdaHandler`](crate::routing::LambdaHandler) to ensure it's present and ensure that you're using "ApiGatewayV1".
+#[derive(Debug, Error)]
+#[error("{inner}")]
+pub struct MissingGatewayContextV1 {
+    inner: MissingGatewayContextTypeV1,
+}
+
+impl<Protocol> IntoResponse<Protocol> for MissingGatewayContextV1 {
+    fn into_response(self) -> http::Response<BoxBody> {
+        internal_server_error()
     }
 }
 
 impl<P> FromParts<P> for ApiGatewayProxyRequestContext {
-    type Rejection = MissingExtension;
+    type Rejection = MissingGatewayContextV1;
 
     fn from_parts(parts: &mut http::request::Parts) -> Result<Self, Self::Rejection> {
-        let Extension(context) = <Extension<RequestContext> as FromParts<P>>::from_parts(parts)?;
+        let context = parts.extensions.remove().ok_or(MissingGatewayContextV1 {
+            inner: MissingGatewayContextTypeV1::MissingRequestContext,
+        })?;
         if let RequestContext::ApiGatewayV1(context) = context {
             Ok(context)
         } else {
-            Err(MissingExtension)
+            Err(MissingGatewayContextV1 {
+                inner: MissingGatewayContextTypeV1::VersionMismatch,
+            })
         }
     }
 }
 
+#[derive(Debug, Error)]
+enum MissingGatewayContextTypeV2 {
+    #[error("`RequestContext` is not present in the `http::Request` extensions - consider using `aws_smithy_http_server::routing::LambdaHandler`")]
+    MissingRequestContext,
+    #[error("`RequestContext::ApiGatewayV1` is present in the `http::Request` extensions - consider using the `aws_smithy_http_server::request::lambda::ApiGatewayProxyRequestContext` extractor")]
+    VersionMismatch,
+}
+
+/// The [`RequestContext::ApiGatewayV2`] was not found in the [`http::Request`] extensions.
+///
+/// Use [`LambdaHandler`](crate::routing::LambdaHandler) to ensure it's present and ensure that you're using "ApiGatewayV2".
+#[derive(Debug, Error)]
+#[error("{inner}")]
+pub struct MissingGatewayContextV2 {
+    inner: MissingGatewayContextTypeV2,
+}
+
+impl<Protocol> IntoResponse<Protocol> for MissingGatewayContextV2 {
+    fn into_response(self) -> http::Response<BoxBody> {
+        internal_server_error()
+    }
+}
+
 impl<P> FromParts<P> for ApiGatewayV2httpRequestContext {
-    type Rejection = MissingExtension;
+    type Rejection = MissingGatewayContextV2;
 
     fn from_parts(parts: &mut http::request::Parts) -> Result<Self, Self::Rejection> {
-        let Extension(context) = <Extension<RequestContext> as FromParts<P>>::from_parts(parts)?;
+        let context = parts.extensions.remove().ok_or(MissingGatewayContextV2 {
+            inner: MissingGatewayContextTypeV2::MissingRequestContext,
+        })?;
         if let RequestContext::ApiGatewayV2(context) = context {
             Ok(context)
         } else {
-            Err(MissingExtension)
+            Err(MissingGatewayContextV2 {
+                inner: MissingGatewayContextTypeV2::VersionMismatch,
+            })
         }
     }
 }
diff --git a/rust-runtime/aws-smithy-http-server/src/request/mod.rs b/rust-runtime/aws-smithy-http-server/src/request/mod.rs
index 6f3e0429ca..77369b871b 100644
--- a/rust-runtime/aws-smithy-http-server/src/request/mod.rs
+++ b/rust-runtime/aws-smithy-http-server/src/request/mod.rs
@@ -46,9 +46,13 @@ use futures_util::{
     future::{try_join, MapErr, MapOk, TryJoin},
     TryFutureExt,
 };
-use http::{request::Parts, Extensions, HeaderMap, Request, Uri};
+use http::{request::Parts, Extensions, HeaderMap, Request, StatusCode, Uri};
 
-use crate::{rejection::any_rejections, response::IntoResponse};
+use crate::{
+    body::{empty, BoxBody},
+    rejection::any_rejections,
+    response::IntoResponse,
+};
 
 pub mod connect_info;
 pub mod extension;
@@ -56,6 +60,12 @@ pub mod extension;
 #[cfg_attr(docsrs, doc(cfg(feature = "aws-lambda")))]
 pub mod lambda;
 
+fn internal_server_error() -> http::Response<BoxBody> {
+    let mut response = http::Response::new(empty());
+    *response.status_mut() = StatusCode::INTERNAL_SERVER_ERROR;
+    response
+}
+
 #[doc(hidden)]
 #[derive(Debug)]
 pub struct RequestParts<B> {