diff --git a/internal/common/serve/spa.go b/internal/common/serve/spa.go
new file mode 100644
index 00000000000..30d9c654db6
--- /dev/null
+++ b/internal/common/serve/spa.go
@@ -0,0 +1,41 @@
+package serve
+
+import (
+	"errors"
+	"io/fs"
+	"net/http"
+	"strings"
+)
+
+const indexHTMLPage = "index.html"
+
+// SinglePageApplicationHandler handles requests for a single-page application front end. It prevents caching of
+// index.html responses and defers handling of file paths which cannot be found to the front end by serving index.html
+// in such cases.
+func SinglePageApplicationHandler(fsys http.FileSystem) http.Handler {
+	return http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+		if shouldServeIndexHTML(fsys, r.URL.Path) {
+			r.URL.Path = "/"
+			// Prevent caching when serving index.html. Its content determines the version of the JS/CSS
+			// bundle, and we want to prevent the user from accessing a stale bundle.
+			w.Header().Set("Cache-Control", "no-store, must-revalidate")
+		}
+
+		http.FileServer(fsys).ServeHTTP(w, r)
+	})
+}
+
+func shouldServeIndexHTML(fsys http.FileSystem, urlPath string) bool {
+	trimmedURLPath := strings.TrimPrefix(urlPath, "/")
+
+	// Serve index.html when the file cannot be found - client-side routing in the SPA handles such cases.
+	if _, err := fsys.Open(trimmedURLPath); errors.Is(err, fs.ErrNotExist) {
+		return true
+	}
+
+	if trimmedURLPath == "" || trimmedURLPath == indexHTMLPage {
+		return true
+	}
+
+	return false
+}
diff --git a/internal/common/serve/static.go b/internal/common/serve/static.go
index 355ae05d8db..3c5a12bb3a5 100644
--- a/internal/common/serve/static.go
+++ b/internal/common/serve/static.go
@@ -1,7 +1,6 @@
 package serve
 
 import (
-	"io/fs"
 	"net/http"
 
 	"github.com/pkg/errors"
@@ -9,27 +8,6 @@ import (
 	"github.com/armadaproject/armada/internal/common/armadacontext"
 )
 
-// dirWithIndexFallback is a http.FileSystem that serves the index.html file at
-// the root of dir if the requested file is not found. This behavior differs
-// from http.Dir, which only forwards requests for /a/ to /a/index.html; we need
-// to serve the index.html file at the root of dir if the requested file is not
-// found, so that the frontend can handle routing in those cases.
-type dirWithIndexFallback struct {
-	dir http.Dir
-}
-
-func CreateDirWithIndexFallback(path string) http.FileSystem {
-	return dirWithIndexFallback{http.Dir(path)}
-}
-
-func (d dirWithIndexFallback) Open(name string) (http.File, error) {
-	file, err := d.dir.Open(name)
-	if errors.Is(err, fs.ErrNotExist) {
-		return d.dir.Open("index.html")
-	}
-	return file, err
-}
-
 // ListenAndServe calls server.ListenAndServe().
 // Additionally, it calls server.Shutdown() if ctx is cancelled.
 func ListenAndServe(ctx *armadacontext.Context, server *http.Server) error {
diff --git a/internal/lookout/gen/restapi/configure_lookout.go b/internal/lookout/gen/restapi/configure_lookout.go
index fd6300bf7d5..38307e4234e 100644
--- a/internal/lookout/gen/restapi/configure_lookout.go
+++ b/internal/lookout/gen/restapi/configure_lookout.go
@@ -97,7 +97,7 @@ func setupGlobalMiddleware(apiHandler http.Handler) http.Handler {
 func uiHandler(apiHandler http.Handler) http.Handler {
 	mux := http.NewServeMux()
 
-	mux.Handle("/", setCacheControl(http.FileServer(serve.CreateDirWithIndexFallback("./internal/lookoutui/build"))))
+	mux.Handle("/", serve.SinglePageApplicationHandler(http.Dir("./internal/lookoutui/build")))
 
 	mux.HandleFunc("/config", func(w http.ResponseWriter, _ *http.Request) {
 		w.Header().Set("Content-Type", "application/json")
@@ -112,19 +112,6 @@ func uiHandler(apiHandler http.Handler) http.Handler {
 	return mux
 }
 
-func setCacheControl(fileHandler http.Handler) http.Handler {
-	return http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
-		if r.URL.Path == "/" || r.URL.Path == "/index.html" {
-			// Because the version of index.html determines the version of the
-			// JavaScript bundle, caching index.html would prevent users from
-			// ever picking up new versions of the JavaScript bundle without
-			// manually invalidating the cache.
-			w.Header().Set("Cache-Control", "no-store")
-		}
-		fileHandler.ServeHTTP(w, r)
-	})
-}
-
 func allowCORS(handler http.Handler, corsAllowedOrigins []string) http.Handler {
 	return http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
 		if origin := r.Header.Get("Origin"); origin != "" && slices.Contains(corsAllowedOrigins, origin) {