diff --git a/src/middleware/ember_index_rewrite.rs b/src/middleware/ember_index_rewrite.rs
index fbcc011a8d1..b42b7cab665 100644
--- a/src/middleware/ember_index_rewrite.rs
+++ b/src/middleware/ember_index_rewrite.rs
@@ -2,18 +2,31 @@
 //! with "/api" and the Accept header contains "html".
 
 use super::prelude::*;
+use std::fmt::Write;
 
-use crate::util::RequestProxy;
+use crate::util::{errors::NotFound, AppResponse, Error, RequestProxy};
+
+use conduit::{Body, HandlerResult};
+use reqwest::blocking::Client;
 
 // Can't derive debug because of Handler and Static.
 #[allow(missing_debug_implementations)]
 pub struct EmberIndexRewrite {
     handler: Option<Box<dyn Handler>>,
+    fastboot_client: Option<Client>,
 }
 
 impl Default for EmberIndexRewrite {
     fn default() -> EmberIndexRewrite {
-        EmberIndexRewrite { handler: None }
+        let fastboot_client = match dotenv::var("USE_FASTBOOT") {
+            Ok(val) if val == "staging-experimental" => Some(Client::new()),
+            _ => None,
+        };
+
+        EmberIndexRewrite {
+            handler: None,
+            fastboot_client,
+        }
     }
 }
 
@@ -24,22 +37,65 @@ impl AroundMiddleware for EmberIndexRewrite {
 }
 
 impl Handler for EmberIndexRewrite {
-    fn call(&self, req: &mut dyn RequestExt) -> AfterResult {
-        // If the client is requesting html, then we've only got one page so
-        // rewrite the request.
-        let wants_html = req
-            .headers()
-            .get_all(header::ACCEPT)
-            .iter()
-            .any(|val| val.to_str().unwrap_or_default().contains("html"));
-        // If the route starts with /api, just assume they want the API
-        // response and fall through.
-        let is_api_path = req.path().starts_with("/api");
+    fn call(&self, req: &mut dyn RequestExt) -> HandlerResult {
         let handler = self.handler.as_ref().unwrap();
-        if wants_html && !is_api_path {
-            handler.call(&mut RequestProxy::rewrite_path(req, "/index.html"))
-        } else {
+
+        if req.path().starts_with("/api") {
             handler.call(req)
+        } else {
+            if let Some(client) = &self.fastboot_client {
+                // During local fastboot development, forward requests to the local fastboot server.
+                // In prodution, including when running with fastboot, nginx proxies the requests
+                // to the correct endpoint and requests should never make it here.
+                return proxy_to_fastboot(client, req).map_err(box_error);
+            }
+
+            if req
+                .headers()
+                .get_all(header::ACCEPT)
+                .iter()
+                .any(|val| val.to_str().unwrap_or_default().contains("html"))
+            {
+                // Serve static Ember page to bootstrap the frontend
+                handler.call(&mut RequestProxy::rewrite_path(req, "/index.html"))
+            } else {
+                // Return a 404 to crawlers that don't send `Accept: text/hml`.
+                // This is to preserve legacy behavior and will likely change.
+                // Most of these crawlers probably won't execute our frontend JS anyway, but
+                // it would be nice to bootstrap the app for crawlers that do execute JS.
+                Ok(NotFound.into())
+            }
         }
     }
 }
+
+/// Proxy to the fastboot server in development mode
+///
+/// This handler is somewhat hacky, and is not intended for usage in production.
+///
+/// # Panics
+///
+/// This function can panic and should only be used in development mode.
+fn proxy_to_fastboot(client: &Client, req: &mut dyn RequestExt) -> Result<AppResponse, Error> {
+    if req.method() != conduit::Method::GET {
+        return Err(format!("Only support GET but request method was {}", req.method()).into());
+    }
+
+    let mut url = format!("http://127.0.0.1:9000{}", req.path());
+    if let Some(query) = req.query_string() {
+        write!(url, "?{}", query).map_err(|e| e.to_string())?;
+    }
+    let mut fastboot_response = client
+        .request(req.method().into(), &*url)
+        .headers(req.headers().clone())
+        .send()?;
+    let mut body = Vec::new();
+    fastboot_response.copy_to(&mut body)?;
+
+    let mut builder = Response::builder().status(fastboot_response.status());
+    builder
+        .headers_mut()
+        .unwrap()
+        .extend(fastboot_response.headers().clone());
+    builder.body(Body::from_vec(body)).map_err(Into::into)
+}
diff --git a/src/util/errors.rs b/src/util/errors.rs
index 727cbb99409..c2e087fa12e 100644
--- a/src/util/errors.rs
+++ b/src/util/errors.rs
@@ -226,9 +226,15 @@ impl AppError for InternalAppError {
 #[derive(Debug, Clone, Copy)]
 pub struct NotFound;
 
+impl From<NotFound> for AppResponse {
+    fn from(_: NotFound) -> AppResponse {
+        json_error("Not Found", StatusCode::NOT_FOUND)
+    }
+}
+
 impl AppError for NotFound {
     fn response(&self) -> Option<AppResponse> {
-        Some(json_error("Not Found", StatusCode::NOT_FOUND))
+        Some(NotFound.into())
     }
 }
 
diff --git a/src/util/errors/concrete.rs b/src/util/errors/concrete.rs
index 54491f00a39..54c2d9d0b3a 100644
--- a/src/util/errors/concrete.rs
+++ b/src/util/errors/concrete.rs
@@ -5,6 +5,7 @@ pub enum Error {
     DbConnect(diesel::result::ConnectionError),
     DbQuery(diesel::result::Error),
     DotEnv(dotenv::Error),
+    Http(http::Error),
     Internal(String),
     Io(io::Error),
     JobEnqueue(swirl::EnqueueError),
@@ -20,6 +21,7 @@ impl fmt::Display for Error {
             Error::DbConnect(inner) => inner.fmt(f),
             Error::DbQuery(inner) => inner.fmt(f),
             Error::DotEnv(inner) => inner.fmt(f),
+            Error::Http(inner) => inner.fmt(f),
             Error::Internal(inner) => inner.fmt(f),
             Error::Io(inner) => inner.fmt(f),
             Error::JobEnqueue(inner) => inner.fmt(f),
@@ -47,6 +49,12 @@ impl From<dotenv::Error> for Error {
     }
 }
 
+impl From<http::Error> for Error {
+    fn from(err: http::Error) -> Self {
+        Error::Http(err)
+    }
+}
+
 impl From<String> for Error {
     fn from(err: String) -> Self {
         Error::Internal(err)