diff --git a/modules/openxr/doc_classes/OpenXRExtensionWrapperExtension.xml b/modules/openxr/doc_classes/OpenXRExtensionWrapperExtension.xml
index 79aa547c526..338d6325241 100644
--- a/modules/openxr/doc_classes/OpenXRExtensionWrapperExtension.xml
+++ b/modules/openxr/doc_classes/OpenXRExtensionWrapperExtension.xml
@@ -84,6 +84,12 @@
 				Called right before the OpenXR instance is destroyed.
 			</description>
 		</method>
+		<method name="_on_main_swapchains_created" qualifiers="virtual">
+			<return type="void" />
+			<description>
+				Called right after the main swapchains are (re)created.
+			</description>
+		</method>
 		<method name="_on_pre_render" qualifiers="virtual">
 			<return type="void" />
 			<description>
diff --git a/modules/openxr/extensions/openxr_extension_wrapper.h b/modules/openxr/extensions/openxr_extension_wrapper.h
index ce03df0b30d..8d05657afce 100644
--- a/modules/openxr/extensions/openxr_extension_wrapper.h
+++ b/modules/openxr/extensions/openxr_extension_wrapper.h
@@ -84,6 +84,7 @@ public:
 	// This is when controller data is queried and made available to game logic.
 	virtual void on_process() {}
 	virtual void on_pre_render() {} // `on_pre_render` is called right before we start rendering our XR viewports.
+	virtual void on_main_swapchains_created() {} // `on_main_swapchains_created` is called right after our main swapchains are (re)created.
 	virtual void on_pre_draw_viewport(RID p_render_target) {} // `on_pre_draw_viewport` is called right before we start rendering this viewport
 	virtual void on_post_draw_viewport(RID p_render_target) {} // `on_port_draw_viewport` is called right after we start rendering this viewport (note that on Vulkan draw commands may only be queued)
 
diff --git a/modules/openxr/extensions/openxr_extension_wrapper_extension.cpp b/modules/openxr/extensions/openxr_extension_wrapper_extension.cpp
index 3b31e1b1f66..e09ca484d52 100644
--- a/modules/openxr/extensions/openxr_extension_wrapper_extension.cpp
+++ b/modules/openxr/extensions/openxr_extension_wrapper_extension.cpp
@@ -50,6 +50,7 @@ void OpenXRExtensionWrapperExtension::_bind_methods() {
 	GDVIRTUAL_BIND(_on_session_created, "session");
 	GDVIRTUAL_BIND(_on_process);
 	GDVIRTUAL_BIND(_on_pre_render);
+	GDVIRTUAL_BIND(_on_main_swapchains_created);
 	GDVIRTUAL_BIND(_on_session_destroyed);
 	GDVIRTUAL_BIND(_on_state_idle);
 	GDVIRTUAL_BIND(_on_state_ready);
@@ -198,6 +199,10 @@ void OpenXRExtensionWrapperExtension::on_pre_render() {
 	GDVIRTUAL_CALL(_on_pre_render);
 }
 
+void OpenXRExtensionWrapperExtension::on_main_swapchains_created() {
+	GDVIRTUAL_CALL(_on_main_swapchains_created);
+}
+
 void OpenXRExtensionWrapperExtension::on_session_destroyed() {
 	GDVIRTUAL_CALL(_on_session_destroyed);
 }
diff --git a/modules/openxr/extensions/openxr_extension_wrapper_extension.h b/modules/openxr/extensions/openxr_extension_wrapper_extension.h
index 71d2a57ff89..e37853903b3 100644
--- a/modules/openxr/extensions/openxr_extension_wrapper_extension.h
+++ b/modules/openxr/extensions/openxr_extension_wrapper_extension.h
@@ -86,6 +86,7 @@ public:
 	virtual void on_session_created(const XrSession p_session) override;
 	virtual void on_process() override;
 	virtual void on_pre_render() override;
+	virtual void on_main_swapchains_created() override;
 	virtual void on_session_destroyed() override;
 
 	GDVIRTUAL0(_on_register_metadata);
@@ -95,6 +96,7 @@ public:
 	GDVIRTUAL1(_on_session_created, uint64_t);
 	GDVIRTUAL0(_on_process);
 	GDVIRTUAL0(_on_pre_render);
+	GDVIRTUAL0(_on_main_swapchains_created);
 	GDVIRTUAL0(_on_session_destroyed);
 
 	virtual void on_state_idle() override;
diff --git a/modules/openxr/extensions/openxr_fb_foveation_extension.cpp b/modules/openxr/extensions/openxr_fb_foveation_extension.cpp
index bbdd2e3c8aa..8ce808dd3c9 100644
--- a/modules/openxr/extensions/openxr_fb_foveation_extension.cpp
+++ b/modules/openxr/extensions/openxr_fb_foveation_extension.cpp
@@ -101,7 +101,7 @@ void *OpenXRFBFoveationExtension::set_swapchain_create_info_and_get_next_pointer
 	}
 }
 
-void OpenXRFBFoveationExtension::on_state_ready() {
+void OpenXRFBFoveationExtension::on_main_swapchains_created() {
 	update_profile();
 }
 
@@ -127,26 +127,41 @@ void OpenXRFBFoveationExtension::set_foveation_dynamic(XrFoveationDynamicFB p_fo
 	update_profile();
 }
 
-void OpenXRFBFoveationExtension::update_profile() {
-	if (!is_enabled()) {
+void OpenXRFBFoveationExtension::_update_profile() {
+	// Must be called from rendering thread!
+	ERR_NOT_ON_RENDER_THREAD;
+
+	OpenXRFBFoveationExtension *fov_ext = OpenXRFBFoveationExtension::get_singleton();
+	ERR_FAIL_NULL(fov_ext);
+
+	if (!fov_ext->is_enabled()) {
+		return;
+	}
+
+	OpenXRAPI *openxr_api = OpenXRAPI::get_singleton();
+	ERR_FAIL_NULL(openxr_api);
+
+	XrSwapchain main_color_swapchain = openxr_api->get_color_swapchain();
+	if (main_color_swapchain == XR_NULL_HANDLE) {
+		// Our swapchain hasn't been created yet, we'll call this again once it has.
 		return;
 	}
 
 	XrFoveationLevelProfileCreateInfoFB level_profile_create_info;
 	level_profile_create_info.type = XR_TYPE_FOVEATION_LEVEL_PROFILE_CREATE_INFO_FB;
 	level_profile_create_info.next = nullptr;
-	level_profile_create_info.level = foveation_level;
+	level_profile_create_info.level = fov_ext->foveation_level;
 	level_profile_create_info.verticalOffset = 0.0f;
-	level_profile_create_info.dynamic = foveation_dynamic;
+	level_profile_create_info.dynamic = fov_ext->foveation_dynamic;
 
 	XrFoveationProfileCreateInfoFB profile_create_info;
 	profile_create_info.type = XR_TYPE_FOVEATION_PROFILE_CREATE_INFO_FB;
 	profile_create_info.next = &level_profile_create_info;
 
 	XrFoveationProfileFB foveation_profile;
-	XrResult result = xrCreateFoveationProfileFB(OpenXRAPI::get_singleton()->get_session(), &profile_create_info, &foveation_profile);
+	XrResult result = fov_ext->xrCreateFoveationProfileFB(openxr_api->get_session(), &profile_create_info, &foveation_profile);
 	if (XR_FAILED(result)) {
-		print_line("OpenXR: Unable to create the foveation profile [", OpenXRAPI::get_singleton()->get_error_string(result), "]");
+		print_line("OpenXR: Unable to create the foveation profile [", openxr_api->get_error_string(result), "]");
 		return;
 	}
 
@@ -154,15 +169,15 @@ void OpenXRFBFoveationExtension::update_profile() {
 	foveation_update_state.type = XR_TYPE_SWAPCHAIN_STATE_FOVEATION_FB;
 	foveation_update_state.profile = foveation_profile;
 
-	result = swapchain_update_state_ext->xrUpdateSwapchainFB(OpenXRAPI::get_singleton()->get_color_swapchain(), (XrSwapchainStateBaseHeaderFB *)&foveation_update_state);
+	result = fov_ext->swapchain_update_state_ext->xrUpdateSwapchainFB(main_color_swapchain, (XrSwapchainStateBaseHeaderFB *)&foveation_update_state);
 	if (XR_FAILED(result)) {
-		print_line("OpenXR: Unable to update the swapchain [", OpenXRAPI::get_singleton()->get_error_string(result), "]");
+		print_line("OpenXR: Unable to update the swapchain [", openxr_api->get_error_string(result), "]");
 
 		// We still want to destroy our profile so keep going...
 	}
 
-	result = xrDestroyFoveationProfileFB(foveation_profile);
+	result = fov_ext->xrDestroyFoveationProfileFB(foveation_profile);
 	if (XR_FAILED(result)) {
-		print_line("OpenXR: Unable to destroy the foveation profile [", OpenXRAPI::get_singleton()->get_error_string(result), "]");
+		print_line("OpenXR: Unable to destroy the foveation profile [", openxr_api->get_error_string(result), "]");
 	}
 }
diff --git a/modules/openxr/extensions/openxr_fb_foveation_extension.h b/modules/openxr/extensions/openxr_fb_foveation_extension.h
index 1c5e7227316..84bd7011b52 100644
--- a/modules/openxr/extensions/openxr_fb_foveation_extension.h
+++ b/modules/openxr/extensions/openxr_fb_foveation_extension.h
@@ -60,7 +60,7 @@ public:
 
 	virtual void *set_swapchain_create_info_and_get_next_pointer(void *p_next_pointer) override;
 
-	virtual void on_state_ready() override;
+	virtual void on_main_swapchains_created() override;
 
 	bool is_enabled() const;
 
@@ -82,7 +82,15 @@ private:
 	XrFoveationLevelFB foveation_level = XR_FOVEATION_LEVEL_NONE_FB;
 	XrFoveationDynamicFB foveation_dynamic = XR_FOVEATION_DYNAMIC_DISABLED_FB;
 
-	void update_profile();
+	static void _update_profile();
+
+	void update_profile() {
+		// If we're rendering on a separate thread, we may still be processing the last frame, don't communicate this till we're ready...
+		RenderingServer *rendering_server = RenderingServer::get_singleton();
+		ERR_FAIL_NULL(rendering_server);
+
+		rendering_server->call_on_render_thread(callable_mp_static(&OpenXRFBFoveationExtension::_update_profile));
+	}
 
 	// Enable foveation on this swapchain
 	XrSwapchainCreateInfoFoveationFB swapchain_create_info_foveation_fb;
diff --git a/modules/openxr/openxr_api.cpp b/modules/openxr/openxr_api.cpp
index 32512070d6d..541e3699251 100644
--- a/modules/openxr/openxr_api.cpp
+++ b/modules/openxr/openxr_api.cpp
@@ -1220,6 +1220,10 @@ bool OpenXRAPI::create_main_swapchains(Size2i p_size) {
 		}
 	};
 
+	for (OpenXRExtensionWrapper *wrapper : registered_extension_wrappers) {
+		wrapper->on_main_swapchains_created();
+	}
+
 	return true;
 };