diff --git a/doc/classes/ProjectSettings.xml b/doc/classes/ProjectSettings.xml
index f86ab17b08e..4b2bb3b6e91 100644
--- a/doc/classes/ProjectSettings.xml
+++ b/doc/classes/ProjectSettings.xml
@@ -566,7 +566,7 @@
 			If [code]true[/code], the home indicator is hidden automatically. This only affects iOS devices without a physical home button.
 		</member>
 		<member name="display/window/per_pixel_transparency/allowed" type="bool" setter="" getter="" default="false">
-			If [code]true[/code], allows per-pixel transparency for the window background. This affects performance, so leave it on [code]false[/code] unless you need it.
+			If [code]true[/code], allows per-pixel transparency for the window background. This affects performance, so leave it on [code]false[/code] unless you need it. See also [member display/window/size/transparent] and [member rendering/transparent_background].
 		</member>
 		<member name="display/window/size/always_on_top" type="bool" setter="" getter="" default="false">
 			Forces the main window to be always on top.
@@ -591,8 +591,8 @@
 			[b]Note:[/b] This setting is ignored on iOS.
 		</member>
 		<member name="display/window/size/transparent" type="bool" setter="" getter="" default="false">
-			Main window background can be transparent.
-			[b]Note:[/b] To use transparent splash screen, set [member application/boot_splash/bg_color] to [code]Color(0, 0, 0, 0)[/code].
+			If [code]true[/code], enables a window manager hint that the main window background [i]can[/i] be transparent. This does not make the background actually transparent. For the background to be transparent, the root viewport must also be made transparent by enabling [member rendering/transparent_background].
+			[b]Note:[/b] To use a transparent splash screen, set [member application/boot_splash/bg_color] to [code]Color(0, 0, 0, 0)[/code].
 			[b]Note:[/b] This setting has no effect if [member display/window/per_pixel_transparency/allowed] is set to [code]false[/code].
 		</member>
 		<member name="display/window/size/viewport_height" type="int" setter="" getter="" default="648">
@@ -2202,6 +2202,9 @@
 			If [code]true[/code], the texture importer will import VRAM-compressed textures using the S3 Texture Compression algorithm. This algorithm is only supported on desktop platforms and consoles.
 			[b]Note:[/b] Changing this setting does [i]not[/i] impact textures that were already imported before. To make this setting apply to textures that were already imported, exit the editor, remove the [code].godot/imported/[/code] folder located inside the project folder then restart the editor (see [member application/config/use_hidden_project_data_directory]).
 		</member>
+		<member name="rendering/transparent_background" type="bool" setter="" getter="" default="false">
+			If [code]true[/code], enables [member Viewport.transparent_bg] on the root viewport. This allows per-pixel transparency to be effective after also enabling [member display/window/size/transparent] and [member display/window/per_pixel_transparency/allowed].
+		</member>
 		<member name="rendering/vrs/mode" type="int" setter="" getter="" default="0">
 			Set the default Variable Rate Shading (VRS) mode for the main viewport. See [member Viewport.vrs_mode] to change this at runtime, and [enum Viewport.VRSMode] for possible values.
 		</member>
diff --git a/editor/plugins/node_3d_editor_plugin.cpp b/editor/plugins/node_3d_editor_plugin.cpp
index 7a213979105..70489f08419 100644
--- a/editor/plugins/node_3d_editor_plugin.cpp
+++ b/editor/plugins/node_3d_editor_plugin.cpp
@@ -2400,6 +2400,9 @@ void Node3DEditorViewport::_project_settings_changed() {
 	const bool use_taa = GLOBAL_GET("rendering/anti_aliasing/quality/use_taa");
 	viewport->set_use_taa(use_taa);
 
+	const bool transparent_background = GLOBAL_GET("rendering/transparent_background");
+	viewport->set_transparent_background(transparent_background);
+
 	const bool use_debanding = GLOBAL_GET("rendering/anti_aliasing/quality/use_debanding");
 	viewport->set_use_debanding(use_debanding);
 
diff --git a/scene/main/scene_tree.cpp b/scene/main/scene_tree.cpp
index af481749d57..64eb3b879b6 100644
--- a/scene/main/scene_tree.cpp
+++ b/scene/main/scene_tree.cpp
@@ -1390,6 +1390,9 @@ SceneTree::SceneTree() {
 	ProjectSettings::get_singleton()->set_custom_property_info("rendering/anti_aliasing/quality/msaa_3d", PropertyInfo(Variant::INT, "rendering/anti_aliasing/quality/msaa_3d", PROPERTY_HINT_ENUM, String::utf8("Disabled (Fastest),2× (Average),4× (Slow),8× (Slowest)")));
 	root->set_msaa_3d(Viewport::MSAA(msaa_mode_3d));
 
+	const bool transparent_background = GLOBAL_DEF("rendering/transparent_background", false);
+	root->set_transparent_background(transparent_background);
+
 	const int ssaa_mode = GLOBAL_DEF_BASIC("rendering/anti_aliasing/quality/screen_space_aa", 0);
 	ProjectSettings::get_singleton()->set_custom_property_info("rendering/anti_aliasing/quality/screen_space_aa", PropertyInfo(Variant::INT, "rendering/anti_aliasing/quality/screen_space_aa", PROPERTY_HINT_ENUM, "Disabled (Fastest),FXAA (Fast)"));
 	root->set_screen_space_aa(Viewport::ScreenSpaceAA(ssaa_mode));