diff --git a/release/scripts/startup/bl_ui/space_userpref.py b/release/scripts/startup/bl_ui/space_userpref.py
index 8db0689ad9c..814e527cbc5 100644
--- a/release/scripts/startup/bl_ui/space_userpref.py
+++ b/release/scripts/startup/bl_ui/space_userpref.py
@@ -210,7 +210,7 @@ class USERPREF_PT_interface_editors(PreferencePanel):
 
         flow = layout.grid_flow(row_major=False, columns=0, even_columns=True, even_rows=False, align=False)
 
-        flow.row().prop(view, "header_align_default", expand=True)
+        flow.row().prop(view, "header_align")
         flow.prop(system, "use_region_overlap")
         flow.prop(view, "show_layout_ui", text="Corner Splitting")
         flow.prop(view, "color_picker_type")
diff --git a/source/blender/blenkernel/BKE_screen.h b/source/blender/blenkernel/BKE_screen.h
index 60cfc15a928..d064929848d 100644
--- a/source/blender/blenkernel/BKE_screen.h
+++ b/source/blender/blenkernel/BKE_screen.h
@@ -357,4 +357,6 @@ void BKE_screen_remove_double_scredges(struct bScreen *sc);
 void BKE_screen_remove_unused_scredges(struct bScreen *sc);
 void BKE_screen_remove_unused_scrverts(struct bScreen *sc);
 
+void BKE_screen_header_alignment_reset(struct bScreen *screen);
+
 #endif
diff --git a/source/blender/blenkernel/intern/screen.c b/source/blender/blenkernel/intern/screen.c
index 2f1393e43d2..af3384d2023 100644
--- a/source/blender/blenkernel/intern/screen.c
+++ b/source/blender/blenkernel/intern/screen.c
@@ -846,3 +846,19 @@ bool BKE_screen_is_used(const bScreen *screen)
 {
 	return (screen->winid != 0);
 }
+
+void BKE_screen_header_alignment_reset(bScreen *screen)
+{
+	int alignment = (U.uiflag & USER_HEADER_BOTTOM) ? RGN_ALIGN_BOTTOM : RGN_ALIGN_TOP;
+	for (ScrArea *sa = screen->areabase.first; sa; sa = sa->next) {
+		for (ARegion *ar = sa->regionbase.first; ar; ar = ar->next) {
+			if (ar->regiontype == RGN_TYPE_HEADER) {
+				if (ELEM(sa->spacetype, SPACE_FILE, SPACE_USERPREF, SPACE_OUTLINER, SPACE_BUTS)) {
+					ar->alignment = RGN_ALIGN_TOP;
+					continue;
+				}
+				ar->alignment = alignment;
+			}
+		}
+	}
+}
diff --git a/source/blender/blenloader/intern/versioning_userdef.c b/source/blender/blenloader/intern/versioning_userdef.c
index 6fa86a06e06..2950af41e1f 100644
--- a/source/blender/blenloader/intern/versioning_userdef.c
+++ b/source/blender/blenloader/intern/versioning_userdef.c
@@ -459,7 +459,7 @@ void BLO_version_defaults_userpref_blend(Main *bmain, UserDef *userdef)
 		        USER_FLAG_DEPRECATED_4);
 
 		userdef->uiflag &= ~(
-		        USER_UIFLAG_DEPRECATED_8 |
+		        USER_HEADER_OVERRIDE |
 		        USER_UIFLAG_DEPRECATED_12 |
 		        USER_UIFLAG_DEPRECATED_22);
 	}
diff --git a/source/blender/makesdna/DNA_userdef_types.h b/source/blender/makesdna/DNA_userdef_types.h
index 3acdf99a79f..0485a81d6c2 100644
--- a/source/blender/makesdna/DNA_userdef_types.h
+++ b/source/blender/makesdna/DNA_userdef_types.h
@@ -866,7 +866,7 @@ typedef enum eUserpref_UI_Flag {
 	USER_PLAINMENUS             = (1 << 5),
 	USER_LOCK_CURSOR_ADJUST     = (1 << 6),
 	USER_HEADER_BOTTOM          = (1 << 7),
-	USER_UIFLAG_DEPRECATED_8    = (1 << 8),  /* cleared */
+	USER_HEADER_OVERRIDE        = (1 << 8),
 	USER_MENUOPENAUTO           = (1 << 9),
 	USER_DEPTH_CURSOR           = (1 << 10),
 	USER_AUTOPERSP              = (1 << 11),
diff --git a/source/blender/makesrna/intern/rna_userdef.c b/source/blender/makesrna/intern/rna_userdef.c
index 578779e18f5..96441c208c8 100644
--- a/source/blender/makesrna/intern/rna_userdef.c
+++ b/source/blender/makesrna/intern/rna_userdef.c
@@ -101,6 +101,7 @@ static const EnumPropertyItem rna_enum_studio_light_type_items[] = {
 #include "BKE_mesh_runtime.h"
 #include "BKE_pbvh.h"
 #include "BKE_paint.h"
+#include "BKE_screen.h"
 
 #include "DEG_depsgraph.h"
 
@@ -152,6 +153,16 @@ static void rna_userdef_update_ui(Main *UNUSED(bmain), Scene *UNUSED(scene), Poi
 	WM_main_add_notifier(NC_SCREEN | NA_EDITED, NULL);    /* refresh region sizes */
 }
 
+static void rna_userdef_update_ui_header_default(Main *bmain, Scene *scene, PointerRNA *ptr)
+{
+	if (U.uiflag & USER_HEADER_OVERRIDE) {
+		for (bScreen *screen = bmain->screen.first; screen; screen = screen->id.next) {
+			BKE_screen_header_alignment_reset(screen);
+		}
+	}
+	rna_userdef_update_ui(bmain, scene, ptr);
+}
+
 static void rna_userdef_language_update(Main *UNUSED(bmain), Scene *UNUSED(scene), PointerRNA *UNUSED(ptr))
 {
 	BLF_cache_clear();
@@ -3853,15 +3864,16 @@ static void rna_def_userdef_view(BlenderRNA *brna)
 	                         "no matter opening direction");
 
 	static const EnumPropertyItem header_align_default_items[] = {
-		{0, "TOP", 0, "Top", ""},
-		{USER_HEADER_BOTTOM, "BOTTOM", 0, "Bottom", ""},
+		{0, "NONE", 0, "From File", ""},
+		{USER_HEADER_OVERRIDE, "TOP", 0, "Top", ""},
+		{USER_HEADER_OVERRIDE | USER_HEADER_BOTTOM, "BOTTOM", 0, "Bottom", ""},
 		{0, NULL, 0, NULL, NULL},
 	};
-	prop = RNA_def_property(srna, "header_align_default", PROP_ENUM, PROP_NONE);
+	prop = RNA_def_property(srna, "header_align", PROP_ENUM, PROP_NONE);
 	RNA_def_property_enum_items(prop, header_align_default_items);
 	RNA_def_property_enum_bitflag_sdna(prop, NULL, "uiflag");
 	RNA_def_property_ui_text(prop, "Header Position", "Default header position for new space-types");
-	RNA_def_property_update(prop, 0, "rna_userdef_update");
+	RNA_def_property_update(prop, 0, "rna_userdef_update_ui_header_default");
 
 	static const EnumPropertyItem text_hinting_items[] = {
 		{0, "AUTO", 0, "Auto", ""},
diff --git a/source/blender/windowmanager/intern/wm_files.c b/source/blender/windowmanager/intern/wm_files.c
index 2de21d756c6..ddc0986f7b8 100644
--- a/source/blender/windowmanager/intern/wm_files.c
+++ b/source/blender/windowmanager/intern/wm_files.c
@@ -488,6 +488,13 @@ static void wm_file_read_post(
 	DEG_on_visible_update(bmain, true);
 	wm_event_do_depsgraph(C);
 
+	if (U.uiflag & USER_HEADER_OVERRIDE) {
+		for (bScreen *screen = bmain->screen.first; screen; screen = screen->id.next) {
+			BKE_screen_header_alignment_reset(screen);
+		}
+		WM_main_add_notifier(NC_SCREEN | NA_EDITED, NULL);
+	}
+
 	ED_editors_init(C);
 
 #ifdef WITH_PYTHON