diff --git a/source/blender/blenkernel/BKE_screen.hh b/source/blender/blenkernel/BKE_screen.hh
index 0200155d580..a178947a6c9 100644
--- a/source/blender/blenkernel/BKE_screen.hh
+++ b/source/blender/blenkernel/BKE_screen.hh
@@ -233,6 +233,12 @@ struct ARegionType {
   /* return context data */
   bContextDataCallback context;
 
+  /**
+   * Called on every frame in which the region's poll succeeds, regardless of visibility, before
+   * drawing, visibility evaluation and initialization. Allows the region to override visibility.
+   */
+  void (*on_poll_success)(const bContext *C, ARegion *region);
+
   /**
    * Called whenever the user changes the region's size. Not called when the size is changed
    * through other means, like to adjust for a scaled down window.
@@ -516,6 +522,7 @@ enum AssetShelfTypeFlag {
   /** Do not trigger asset dragging on drag events. Drag events can be overridden with custom
    * keymap items then. */
   ASSET_SHELF_TYPE_FLAG_NO_ASSET_DRAG = (1 << 0),
+  ASSET_SHELF_TYPE_FLAG_DEFAULT_VISIBLE = (1 << 1),
 
   ASSET_SHELF_TYPE_FLAG_MAX
 };
diff --git a/source/blender/editors/asset/ED_asset_shelf.hh b/source/blender/editors/asset/ED_asset_shelf.hh
index cb08ad95d7b..10115c8011f 100644
--- a/source/blender/editors/asset/ED_asset_shelf.hh
+++ b/source/blender/editors/asset/ED_asset_shelf.hh
@@ -47,6 +47,7 @@ void region_on_user_resize(const ARegion *region);
 void region_listen(const wmRegionListenerParams *params);
 void region_layout(const bContext *C, ARegion *region);
 void region_draw(const bContext *C, ARegion *region);
+void region_on_poll_success(const bContext *C, ARegion *region);
 void region_blend_read_data(BlendDataReader *reader, ARegion *region);
 void region_blend_write(BlendWriter *writer, ARegion *region);
 int region_prefsizey();
diff --git a/source/blender/editors/asset/intern/asset_shelf.cc b/source/blender/editors/asset/intern/asset_shelf.cc
index 86db72d3517..33f48a347ae 100644
--- a/source/blender/editors/asset/intern/asset_shelf.cc
+++ b/source/blender/editors/asset/intern/asset_shelf.cc
@@ -131,12 +131,15 @@ static void activate_shelf(RegionAssetShelf &shelf_regiondata, AssetShelf &shelf
  *
  * The returned shelf is guaranteed to have its #AssetShelf.type pointer set.
  *
+ * \param on_create: Function called when a new asset shelf is created (case 3).
+ *
  * \return A non-owning pointer to the now active shelf. Might be null if no shelf is valid in
  *         current context (all polls failed).
  */
 static AssetShelf *update_active_shelf(const bContext &C,
                                        const SpaceType &space_type,
-                                       RegionAssetShelf &shelf_regiondata)
+                                       RegionAssetShelf &shelf_regiondata,
+                                       FunctionRef<void(AssetShelf &new_shelf)> on_create)
 {
   /* Note: Don't access #AssetShelf.type directly, use #type_ensure(). */
 
@@ -170,6 +173,9 @@ static AssetShelf *update_active_shelf(const bContext &C,
       BLI_addhead(&shelf_regiondata.shelves, new_shelf);
       /* Moves ownership to the regiondata. */
       activate_shelf(shelf_regiondata, *new_shelf);
+      if (on_create) {
+        on_create(*new_shelf);
+      }
       return new_shelf;
     }
   }
@@ -260,13 +266,13 @@ void region_listen(const wmRegionListenerParams *params)
 
 void region_init(wmWindowManager *wm, ARegion *region)
 {
-  if (!region->regiondata) {
-    region->regiondata = MEM_cnew<RegionAssetShelf>("RegionAssetShelf");
-  }
-  RegionAssetShelf &shelf_regiondata = *RegionAssetShelf::get_from_asset_shelf_region(*region);
+  /* Region-data should've been created by a previously called #region_before_redraw(). */
+  RegionAssetShelf *shelf_regiondata = RegionAssetShelf::get_from_asset_shelf_region(*region);
+  BLI_assert_msg(
+      shelf_regiondata,
+      "Region-data should've been created by a previously called `region_before_redraw()`.");
 
-  /* Active shelf is only set on draw, so this may be null! */
-  AssetShelf *active_shelf = shelf_regiondata.active_shelf;
+  AssetShelf *active_shelf = shelf_regiondata->active_shelf;
 
   UI_view2d_region_reinit(&region->v2d, V2D_COMMONVIEW_PANELS_UI, region->winx, region->winy);
 
@@ -410,17 +416,12 @@ int region_prefsizey()
 
 void region_layout(const bContext *C, ARegion *region)
 {
-  const SpaceLink *space = CTX_wm_space_data(C);
-  SpaceType *space_type = BKE_spacetype_from_id(space->spacetype);
-
   RegionAssetShelf *shelf_regiondata = RegionAssetShelf::get_from_asset_shelf_region(*region);
-  if (!shelf_regiondata) {
-    /* Region-data should've been created by a previously called #region_init(). */
-    BLI_assert_unreachable();
-    return;
-  }
+  BLI_assert_msg(
+      shelf_regiondata,
+      "Region-data should've been created by a previously called `region_before_redraw()`.");
 
-  AssetShelf *active_shelf = update_active_shelf(*C, *space_type, *shelf_regiondata);
+  const AssetShelf *active_shelf = shelf_regiondata->active_shelf;
   if (!active_shelf) {
     return;
   }
@@ -472,6 +473,28 @@ void region_draw(const bContext *C, ARegion *region)
   UI_view2d_scrollers_draw(&region->v2d, nullptr);
 }
 
+void region_on_poll_success(const bContext *C, ARegion *region)
+{
+  RegionAssetShelf *shelf_regiondata = RegionAssetShelf::ensure_from_asset_shelf_region(*region);
+  if (!shelf_regiondata) {
+    BLI_assert_unreachable();
+    return;
+  }
+
+  ScrArea *area = CTX_wm_area(C);
+  update_active_shelf(
+      *C, *area->type, *shelf_regiondata, /*on_create=*/[&](AssetShelf &new_shelf) {
+        /* Update region visibility (`'DEFAULT_VISIBLE'` option). */
+        const int old_flag = region->flag;
+        SET_FLAG_FROM_TEST(region->flag,
+                           (new_shelf.type->flag & ASSET_SHELF_TYPE_FLAG_DEFAULT_VISIBLE) == 0,
+                           RGN_FLAG_HIDDEN);
+        if (old_flag != region->flag) {
+          ED_region_visibility_change_update(const_cast<bContext *>(C), area, region);
+        }
+      });
+}
+
 void header_region_listen(const wmRegionListenerParams *params)
 {
   asset_shelf_region_listen(params);
@@ -486,15 +509,6 @@ void header_region_init(wmWindowManager * /*wm*/, ARegion *region)
 
 void header_region(const bContext *C, ARegion *region)
 {
-  const SpaceLink *space = CTX_wm_space_data(C);
-  SpaceType *space_type = BKE_spacetype_from_id(space->spacetype);
-  const ARegion *main_shelf_region = BKE_area_find_region_type(CTX_wm_area(C),
-                                                               RGN_TYPE_ASSET_SHELF);
-
-  RegionAssetShelf *shelf_regiondata = RegionAssetShelf::get_from_asset_shelf_region(
-      *main_shelf_region);
-  update_active_shelf(*C, *space_type, *shelf_regiondata);
-
   ED_region_header_with_button_sections(C, region, uiButtonSectionsAlign::Bottom);
 }
 
diff --git a/source/blender/editors/asset/intern/asset_shelf_regiondata.cc b/source/blender/editors/asset/intern/asset_shelf_regiondata.cc
index 5cf411e73cd..e2c3b418a49 100644
--- a/source/blender/editors/asset/intern/asset_shelf_regiondata.cc
+++ b/source/blender/editors/asset/intern/asset_shelf_regiondata.cc
@@ -25,6 +25,19 @@ RegionAssetShelf *RegionAssetShelf::get_from_asset_shelf_region(const ARegion &r
   return static_cast<RegionAssetShelf *>(region.regiondata);
 }
 
+RegionAssetShelf *RegionAssetShelf::ensure_from_asset_shelf_region(ARegion &region)
+{
+  if (region.regiontype != RGN_TYPE_ASSET_SHELF) {
+    /* Should only be called on main asset shelf region. */
+    BLI_assert_unreachable();
+    return nullptr;
+  }
+  if (!region.regiondata) {
+    region.regiondata = MEM_cnew<RegionAssetShelf>("RegionAssetShelf");
+  }
+  return static_cast<RegionAssetShelf *>(region.regiondata);
+}
+
 namespace blender::ed::asset::shelf {
 
 RegionAssetShelf *regiondata_duplicate(const RegionAssetShelf *shelf_regiondata)
diff --git a/source/blender/editors/screen/area.cc b/source/blender/editors/screen/area.cc
index d2992ee0fb4..09f4c2fb1d7 100644
--- a/source/blender/editors/screen/area.cc
+++ b/source/blender/editors/screen/area.cc
@@ -2021,6 +2021,9 @@ void ED_area_update_region_sizes(wmWindowManager *wm, wmWindow *win, ScrArea *ar
   area_azone_init(win, screen, area);
 
   LISTBASE_FOREACH (ARegion *, region, &area->regionbase) {
+    if (region->flag & RGN_FLAG_POLL_FAILED) {
+      continue;
+    }
     region_evaulate_visibility(region);
 
     /* region size may have changed, init does necessary adjustments */
diff --git a/source/blender/editors/screen/screen_edit.cc b/source/blender/editors/screen/screen_edit.cc
index 4c1b8af99df..90fb94cf634 100644
--- a/source/blender/editors/screen/screen_edit.cc
+++ b/source/blender/editors/screen/screen_edit.cc
@@ -755,6 +755,9 @@ static void screen_regions_poll(bContext *C, const wmWindow *win, bScreen *scree
       if (region_poll(C, screen, area, region) == false) {
         region->flag |= RGN_FLAG_POLL_FAILED;
       }
+      else if (region->type && region->type->on_poll_success) {
+        region->type->on_poll_success(C, region);
+      }
 
       if (old_region_flag != region->flag) {
         any_changed = true;
diff --git a/source/blender/editors/space_image/space_image.cc b/source/blender/editors/space_image/space_image.cc
index ecfaa592898..42aa7433a51 100644
--- a/source/blender/editors/space_image/space_image.cc
+++ b/source/blender/editors/space_image/space_image.cc
@@ -1200,6 +1200,7 @@ void ED_spacetype_image()
   art->keymapflag = ED_KEYMAP_UI | ED_KEYMAP_ASSET_SHELF | ED_KEYMAP_FRAMES;
   art->duplicate = asset::shelf::region_duplicate;
   art->free = asset::shelf::region_free;
+  art->on_poll_success = asset::shelf::region_on_poll_success;
   art->listener = asset::shelf::region_listen;
   art->poll = asset::shelf::regions_poll;
   art->snap_size = asset::shelf::region_snap;
diff --git a/source/blender/editors/space_view3d/space_view3d.cc b/source/blender/editors/space_view3d/space_view3d.cc
index c3a09b737d6..570b18fd7ee 100644
--- a/source/blender/editors/space_view3d/space_view3d.cc
+++ b/source/blender/editors/space_view3d/space_view3d.cc
@@ -2209,6 +2209,7 @@ void ED_spacetype_view3d()
   art->keymapflag = ED_KEYMAP_UI | ED_KEYMAP_ASSET_SHELF | ED_KEYMAP_FRAMES;
   art->duplicate = asset::shelf::region_duplicate;
   art->free = asset::shelf::region_free;
+  art->on_poll_success = asset::shelf::region_on_poll_success;
   art->listener = asset::shelf::region_listen;
   art->poll = asset::shelf::regions_poll;
   art->snap_size = asset::shelf::region_snap;
diff --git a/source/blender/makesdna/DNA_screen_types.h b/source/blender/makesdna/DNA_screen_types.h
index 972f1a59b2d..32d32c7e7f4 100644
--- a/source/blender/makesdna/DNA_screen_types.h
+++ b/source/blender/makesdna/DNA_screen_types.h
@@ -855,6 +855,8 @@ typedef struct RegionAssetShelf {
   AssetShelf *active_shelf; /* Non-owning. */
 #ifdef __cplusplus
   static RegionAssetShelf *get_from_asset_shelf_region(const ARegion &region);
+  /** Creates the asset shelf region data if necessary, and returns it. */
+  static RegionAssetShelf *ensure_from_asset_shelf_region(ARegion &region);
 #endif
 } RegionAssetShelf;
 
diff --git a/source/blender/makesrna/intern/rna_ui.cc b/source/blender/makesrna/intern/rna_ui.cc
index b10048ec2aa..0f35e8cb3ac 100644
--- a/source/blender/makesrna/intern/rna_ui.cc
+++ b/source/blender/makesrna/intern/rna_ui.cc
@@ -2261,6 +2261,12 @@ static void rna_def_asset_shelf(BlenderRNA *brna)
        "No Asset Dragging",
        "Disable the default asset dragging on drag events. Useful for implementing custom "
        "dragging via custom key-map items"},
+      {ASSET_SHELF_TYPE_FLAG_DEFAULT_VISIBLE,
+       "DEFAULT_VISIBLE",
+       0,
+       "Visible by Default",
+       "Unhide the asset shelf when it's available for the first time, otherwise it will be "
+       "hidden"},
       {0, nullptr, 0, nullptr, nullptr},
   };