diff --git a/src/proto/conn.rs b/src/proto/conn.rs
index c3f8bff0bf..c7999488c2 100644
--- a/src/proto/conn.rs
+++ b/src/proto/conn.rs
@@ -186,7 +186,8 @@ where I: AsyncRead + AsyncWrite,
                     let was_mid_parse = !self.io.read_buf().is_empty();
                     return if was_mid_parse || must_error {
                         debug!("parse error ({}) with {} bytes", e, self.io.read_buf().len());
-                        Err(e)
+                        self.on_parse_error(e)
+                            .map(|()| Async::NotReady)
                     } else {
                         debug!("read eof");
                         Ok(Async::Ready(None))
@@ -213,7 +214,8 @@ where I: AsyncRead + AsyncWrite,
                 Err(e) => {
                     debug!("decoder error = {:?}", e);
                     self.state.close_read();
-                    return Err(e);
+                    return self.on_parse_error(e)
+                        .map(|()| Async::NotReady);
                 }
             };
 
@@ -548,6 +550,27 @@ where I: AsyncRead + AsyncWrite,
         Ok(AsyncSink::Ready)
     }
 
+    // When we get a parse error, depending on what side we are, we might be able
+    // to write a response before closing the connection.
+    //
+    // - Client: there is nothing we can do
+    // - Server: if Response hasn't been written yet, we can send a 4xx response
+    fn on_parse_error(&mut self, err: ::Error) -> ::Result<()> {
+        match self.state.writing {
+            Writing::Init => {
+                if let Some(msg) = T::on_error(&err) {
+                    self.write_head(msg, false);
+                    self.state.error = Some(err);
+                    return Ok(());
+                }
+            }
+            _ => (),
+        }
+
+        // fallback is pass the error back up
+        Err(err)
+    }
+
     fn write_queued(&mut self) -> Poll<(), io::Error> {
         trace!("Conn::write_queued()");
         let state = match self.state.writing {
diff --git a/src/proto/h1/parse.rs b/src/proto/h1/parse.rs
index 0ca640cc68..b0f5df171f 100644
--- a/src/proto/h1/parse.rs
+++ b/src/proto/h1/parse.rs
@@ -150,6 +150,26 @@ impl Http1Transaction for ServerTransaction {
         ret
     }
 
+    fn on_error(err: &::Error) -> Option<MessageHead<Self::Outgoing>> {
+        let status = match err {
+            &::Error::Method |
+            &::Error::Version |
+            &::Error::Header |
+            &::Error::Uri(_) => {
+                StatusCode::BadRequest
+            },
+            &::Error::TooLarge => {
+                StatusCode::RequestHeaderFieldsTooLarge
+            }
+            _ => return None,
+        };
+
+        debug!("sending automatic response ({}) for parse error", status);
+        let mut msg = MessageHead::default();
+        msg.subject = status;
+        Some(msg)
+    }
+
     fn should_error_on_parse_eof() -> bool {
         false
     }
@@ -317,6 +337,11 @@ impl Http1Transaction for ClientTransaction {
         Ok(body)
     }
 
+    fn on_error(_err: &::Error) -> Option<MessageHead<Self::Outgoing>> {
+        // we can't tell the server about any errors it creates
+        None
+    }
+
     fn should_error_on_parse_eof() -> bool {
         true
     }
diff --git a/src/proto/mod.rs b/src/proto/mod.rs
index a562b3804c..54576b44ef 100644
--- a/src/proto/mod.rs
+++ b/src/proto/mod.rs
@@ -149,6 +149,7 @@ pub trait Http1Transaction {
     fn parse(bytes: &mut BytesMut) -> ParseResult<Self::Incoming>;
     fn decoder(head: &MessageHead<Self::Incoming>, method: &mut Option<::Method>) -> ::Result<Option<h1::Decoder>>;
     fn encode(head: MessageHead<Self::Outgoing>, has_body: bool, method: &mut Option<Method>, dst: &mut Vec<u8>) -> ::Result<h1::Encoder>;
+    fn on_error(err: &::Error) -> Option<MessageHead<Self::Outgoing>>;
 
     fn should_error_on_parse_eof() -> bool;
     fn should_read_first() -> bool;
diff --git a/tests/server.rs b/tests/server.rs
index 159271802d..d6a70f4590 100644
--- a/tests/server.rs
+++ b/tests/server.rs
@@ -900,6 +900,64 @@ fn returning_1xx_response_is_error() {
     core.run(fut).unwrap_err();
 }
 
+#[test]
+fn parse_errors_send_4xx_response() {
+    let mut core = Core::new().unwrap();
+    let listener = TcpListener::bind(&"127.0.0.1:0".parse().unwrap(), &core.handle()).unwrap();
+    let addr = listener.local_addr().unwrap();
+
+    thread::spawn(move || {
+        let mut tcp = connect(&addr);
+        tcp.write_all(b"GE T / HTTP/1.1\r\n\r\n").unwrap();
+        let mut buf = [0; 256];
+        tcp.read(&mut buf).unwrap();
+
+        let expected = "HTTP/1.1 400 ";
+        assert_eq!(s(&buf[..expected.len()]), expected);
+    });
+
+    let fut = listener.incoming()
+        .into_future()
+        .map_err(|_| unreachable!())
+        .and_then(|(item, _incoming)| {
+            let (socket, _) = item.unwrap();
+            Http::<hyper::Chunk>::new()
+                .serve_connection(socket, HelloWorld)
+                .map(|_| ())
+        });
+
+    core.run(fut).unwrap_err();
+}
+
+#[test]
+fn illegal_request_length_returns_400_response() {
+    let mut core = Core::new().unwrap();
+    let listener = TcpListener::bind(&"127.0.0.1:0".parse().unwrap(), &core.handle()).unwrap();
+    let addr = listener.local_addr().unwrap();
+
+    thread::spawn(move || {
+        let mut tcp = connect(&addr);
+        tcp.write_all(b"POST / HTTP/1.1\r\nContent-Length: foo\r\n\r\n").unwrap();
+        let mut buf = [0; 256];
+        tcp.read(&mut buf).unwrap();
+
+        let expected = "HTTP/1.1 400 ";
+        assert_eq!(s(&buf[..expected.len()]), expected);
+    });
+
+    let fut = listener.incoming()
+        .into_future()
+        .map_err(|_| unreachable!())
+        .and_then(|(item, _incoming)| {
+            let (socket, _) = item.unwrap();
+            Http::<hyper::Chunk>::new()
+                .serve_connection(socket, HelloWorld)
+                .map(|_| ())
+        });
+
+    core.run(fut).unwrap_err();
+}
+
 #[test]
 fn remote_addr() {
     let server = serve();