diff --git a/shell/platform/linux/BUILD.gn b/shell/platform/linux/BUILD.gn
index 523ea1194899c..0512376aefe7c 100644
--- a/shell/platform/linux/BUILD.gn
+++ b/shell/platform/linux/BUILD.gn
@@ -129,6 +129,7 @@ source_set("flutter_linux") {
     "//flutter/shell/platform/linux/config:gtk",
     "//flutter/shell/platform/linux/config:egl",
     "//flutter/shell/platform/linux/config:wayland-egl",
+    "//flutter/shell/platform/linux/config:x11",
     "//third_party/khronos:khronos_headers",
   ]
 
@@ -172,6 +173,7 @@ executable("flutter_linux_unittests") {
   configs += [
     "//flutter/shell/platform/linux/config:gtk",
     "//flutter/shell/platform/linux/config:wayland-egl",
+    "//flutter/shell/platform/linux/config:x11",
   ]
 
   # Set flag to allow public headers to be directly included (library users should not do this)
diff --git a/shell/platform/linux/config/BUILD.gn b/shell/platform/linux/config/BUILD.gn
index 77402c5315b78..e8fd120e25d3b 100644
--- a/shell/platform/linux/config/BUILD.gn
+++ b/shell/platform/linux/config/BUILD.gn
@@ -5,10 +5,8 @@
 import("//build/config/linux/pkg_config.gni")
 import("//flutter/shell/platform/glfw/config.gni")
 
-if (build_glfw_shell) {
-  pkg_config("x11") {
-    packages = [ "x11" ]
-  }
+pkg_config("x11") {
+  packages = [ "x11" ]
 }
 
 pkg_config("gtk") {
diff --git a/shell/platform/linux/fl_renderer_x11.cc b/shell/platform/linux/fl_renderer_x11.cc
index 2c646b16ca223..2e9d7c147996a 100644
--- a/shell/platform/linux/fl_renderer_x11.cc
+++ b/shell/platform/linux/fl_renderer_x11.cc
@@ -5,14 +5,30 @@
 #include "fl_renderer_x11.h"
 #ifdef GDK_WINDOWING_X11
 
+#include <X11/X.h>
+
 #include "flutter/shell/platform/linux/egl_utils.h"
 
 struct _FlRendererX11 {
   FlRenderer parent_instance;
+
+  // Connection to the X server.
+  Display* display;
 };
 
 G_DEFINE_TYPE(FlRendererX11, fl_renderer_x11, fl_renderer_get_type())
 
+static void fl_renderer_x11_dispose(GObject* object) {
+  FlRendererX11* self = FL_RENDERER_X11(object);
+
+  if (self->display != nullptr) {
+    XCloseDisplay(self->display);
+    self->display = nullptr;
+  }
+
+  G_OBJECT_CLASS(fl_renderer_x11_parent_class)->dispose(object);
+}
+
 // Implements FlRenderer::setup_window_attr.
 static gboolean fl_renderer_x11_setup_window_attr(
     FlRenderer* renderer,
@@ -50,11 +66,17 @@ static gboolean fl_renderer_x11_setup_window_attr(
 
 // Implements FlRenderer::create_display.
 static EGLDisplay fl_renderer_x11_create_display(FlRenderer* renderer) {
-  // Note the use of EGL_DEFAULT_DISPLAY rather than sharing the existing
-  // display connection from GTK. This is because this EGL display is going to
-  // be accessed by a thread from Flutter. The GTK/X11 display connection is not
-  // thread safe and would cause a crash.
-  return eglGetDisplay(EGL_DEFAULT_DISPLAY);
+  FlRendererX11* self = FL_RENDERER_X11(renderer);
+
+  // Create a dedicated connection to the X server because the EGL calls are
+  // made from Flutter on a different thread to GTK. Re-using the existing
+  // GTK X11 connection would crash as Xlib is not thread safe.
+  if (self->display == nullptr) {
+    Display* display = gdk_x11_get_default_xdisplay();
+    self->display = XOpenDisplay(DisplayString(display));
+  }
+
+  return eglGetDisplay(self->display);
 }
 
 // Implements FlRenderer::create_surfaces.
@@ -99,6 +121,7 @@ static gboolean fl_renderer_x11_create_surfaces(FlRenderer* renderer,
 }
 
 static void fl_renderer_x11_class_init(FlRendererX11Class* klass) {
+  G_OBJECT_CLASS(klass)->dispose = fl_renderer_x11_dispose;
   FL_RENDERER_CLASS(klass)->setup_window_attr =
       fl_renderer_x11_setup_window_attr;
   FL_RENDERER_CLASS(klass)->create_display = fl_renderer_x11_create_display;