diff --git a/agent/http.go b/agent/http.go
index c07d6df5db..4a84260921 100644
--- a/agent/http.go
+++ b/agent/http.go
@@ -322,9 +322,25 @@ func (s *HTTPServer) handler(enableDebug bool) http.Handler {
 			fs := assetFS()
 			uifs = fs
 		}
+
 		uifs = &redirectFS{fs: &templatedIndexFS{fs: uifs, templateVars: s.GenerateHTMLTemplateVars}}
-		mux.Handle("/robots.txt", http.FileServer(uifs))
-		mux.Handle(s.agent.config.UIContentPath, http.StripPrefix(s.agent.config.UIContentPath, http.FileServer(uifs)))
+		// create a http handler using the ui file system
+		// and the headers specified by the http_config.response_headers user config
+		uifsWithHeaders := serveHandlerWithHeaders(
+			http.FileServer(uifs),
+			s.agent.config.HTTPResponseHeaders,
+		)
+		mux.Handle(
+			"/robots.txt",
+			uifsWithHeaders,
+		)
+		mux.Handle(
+			s.agent.config.UIContentPath,
+			http.StripPrefix(
+				s.agent.config.UIContentPath,
+				uifsWithHeaders,
+			),
+		)
 	}
 
 	// Wrap the whole mux with a handler that bans URLs with non-printable
@@ -752,6 +768,14 @@ func setHeaders(resp http.ResponseWriter, headers map[string]string) {
 	}
 }
 
+// serveHandlerWithHeaders is used to serve a http.Handler with the specified headers
+func serveHandlerWithHeaders(h http.Handler, headers map[string]string) http.HandlerFunc {
+	return func(resp http.ResponseWriter, req *http.Request) {
+		setHeaders(resp, headers)
+		h.ServeHTTP(resp, req)
+	}
+}
+
 // parseWait is used to parse the ?wait and ?index query params
 // Returns true on error
 func parseWait(resp http.ResponseWriter, req *http.Request, b structs.QueryOptionsCompat) bool {
diff --git a/agent/http_test.go b/agent/http_test.go
index 5fe80c3045..b02a6982c7 100644
--- a/agent/http_test.go
+++ b/agent/http_test.go
@@ -431,6 +431,36 @@ func TestHTTPAPIResponseHeaders(t *testing.T) {
 		t.Fatalf("bad X-XSS-Protection header: expected %q, got %q", "1; mode=block", xss)
 	}
 }
+func TestUIResponseHeaders(t *testing.T) {
+	t.Parallel()
+	a := NewTestAgent(t, t.Name(), `
+		http_config {
+			response_headers = {
+				"Access-Control-Allow-Origin" = "*"
+				"X-Frame-Options" = "SAMEORIGIN"
+			}
+		}
+	`)
+	defer a.Shutdown()
+
+	resp := httptest.NewRecorder()
+	handler := func(resp http.ResponseWriter, req *http.Request) (interface{}, error) {
+		return nil, nil
+	}
+
+	req, _ := http.NewRequest("GET", "/ui", nil)
+	a.srv.wrap(handler, []string{"GET"})(resp, req)
+
+	origin := resp.Header().Get("Access-Control-Allow-Origin")
+	if origin != "*" {
+		t.Fatalf("bad Access-Control-Allow-Origin: expected %q, got %q", "*", origin)
+	}
+
+	frameOptions := resp.Header().Get("X-Frame-Options")
+	if frameOptions != "SAMEORIGIN" {
+		t.Fatalf("bad X-XSS-Protection header: expected %q, got %q", "SAMEORIGIN", frameOptions)
+	}
+}
 
 func TestContentTypeIsJSON(t *testing.T) {
 	t.Parallel()