diff --git a/agent/ui_endpoint_test.go b/agent/ui_endpoint_test.go
index 7338417e4..006aa841d 100644
--- a/agent/ui_endpoint_test.go
+++ b/agent/ui_endpoint_test.go
@@ -28,18 +28,20 @@ func TestUiIndex(t *testing.T) {
 
 	// Make the server
 	a := NewTestAgent(t, `
-		ui_dir = "`+uiDir+`"
+		ui_config {
+			dir = "`+uiDir+`"
+		}
 	`)
 	defer a.Shutdown()
 	testrpc.WaitForLeader(t, a.RPC, "dc1")
 
 	// Create file
 	path := filepath.Join(a.Config.UIConfig.Dir, "my-file")
-	if err := ioutil.WriteFile(path, []byte("test"), 0777); err != nil {
+	if err := ioutil.WriteFile(path, []byte("test"), 0644); err != nil {
 		t.Fatalf("err: %v", err)
 	}
 
-	// Register node
+	// Request the custom file
 	req, _ := http.NewRequest("GET", "/ui/my-file", nil)
 	req.URL.Scheme = "http"
 	req.URL.Host = a.HTTPAddr()
diff --git a/agent/uiserver/ui_template_data.go b/agent/uiserver/ui_template_data.go
index cb80f4235..13852ba68 100644
--- a/agent/uiserver/ui_template_data.go
+++ b/agent/uiserver/ui_template_data.go
@@ -35,6 +35,9 @@ func uiTemplateDataFromConfig(cfg *config.RuntimeConfig) (map[string]interface{}
 	}
 
 	err := uiTemplateDataFromConfigEnterprise(cfg, d, uiCfg)
+	if err != nil {
+		return nil, err
+	}
 
 	// Render uiCfg down to JSON ready to inject into the template
 	bs, err := json.Marshal(uiCfg)
diff --git a/agent/uiserver/uiserver.go b/agent/uiserver/uiserver.go
index 2c3d807fe..436f847a8 100644
--- a/agent/uiserver/uiserver.go
+++ b/agent/uiserver/uiserver.go
@@ -88,22 +88,36 @@ func (h *Handler) ReloadConfig(newCfg *config.RuntimeConfig) error {
 
 	// Render a new index.html with the new config values ready to serve.
 	buf, info, err := renderIndex(newCfg, fs)
-	if err != nil {
+	if _, ok := err.(*os.PathError); ok && newCfg.UIConfig.Dir != "" {
+		// A Path error indicates that there is no index.html. This could happen if
+		// the user configured their own UI dir and is serving something that is not
+		// our usual UI. This won't work perfectly because our uiserver will still
+		// redirect everything to the UI but we shouldn't fail the entire UI server
+		// with a 500 in this case. Partly that's just bad UX and partly it's a
+		// breaking change although quite an edge case. Instead, continue but just
+		// return a 404 response for the index.html and log a warning.
+		h.logger.Warn("ui_config.dir does not contain an index.html. Index templating and redirects to index.html are disabled.")
+	} else if err != nil {
 		return err
 	}
 
-	// Create a new fs that serves the rendered index file or falls back to the
-	// underlying FS.
-	fs = &bufIndexFS{
-		fs:            fs,
-		indexRendered: buf,
-		indexInfo:     info,
+	// buf can be nil in the PathError case above. We should skip this part but
+	// still serve the rest of the files in that case.
+	if buf != nil {
+		// Create a new fs that serves the rendered index file or falls back to the
+		// underlying FS.
+		fs = &bufIndexFS{
+			fs:            fs,
+			indexRendered: buf,
+			indexInfo:     info,
+		}
+
+		// Wrap the buffering FS our redirect FS. This needs to happen later so that
+		// redirected requests for /index.html get served the rendered version not the
+		// original.
+		fs = &redirectFS{fs: fs}
 	}
 
-	// Wrap the buffering FS our redirect FS. This needs to happen later so that
-	// redirected requests for /index.html get served the rendered version not the
-	// original.
-	fs = &redirectFS{fs: fs}
 	newState.srv = http.FileServer(fs)
 
 	// Store the new state
diff --git a/agent/uiserver/uiserver_test.go b/agent/uiserver/uiserver_test.go
index 6ab43eb73..ea6f623b3 100644
--- a/agent/uiserver/uiserver_test.go
+++ b/agent/uiserver/uiserver_test.go
@@ -2,9 +2,12 @@ package uiserver
 
 import (
 	"encoding/json"
+	"io/ioutil"
 	"net/http"
 	"net/http/httptest"
 	"net/url"
+	"os"
+	"path/filepath"
 	"regexp"
 	"testing"
 
@@ -228,3 +231,23 @@ func TestReload(t *testing.T) {
 		require.Contains(t, rec.Body.String(), "exotic-metrics-provider-name")
 	}
 }
+
+func TestCustomDir(t *testing.T) {
+	uiDir := testutil.TempDir(t, "consul-uiserver")
+	defer os.RemoveAll(uiDir)
+
+	path := filepath.Join(uiDir, "test-file")
+	require.NoError(t, ioutil.WriteFile(path, []byte("test"), 0644))
+
+	cfg := basicUIEnabledConfig()
+	cfg.UIConfig.Dir = uiDir
+	h := NewHandler(cfg, testutil.Logger(t))
+
+	req := httptest.NewRequest("GET", "/test-file", nil)
+	rec := httptest.NewRecorder()
+
+	h.ServeHTTP(rec, req)
+
+	require.Equal(t, http.StatusOK, rec.Code)
+	require.Contains(t, rec.Body.String(), "test")
+}