diff --git a/source/blender/blenkernel/BKE_screen.hh b/source/blender/blenkernel/BKE_screen.hh
index 2dc4226e18c..b05a4479872 100644
--- a/source/blender/blenkernel/BKE_screen.hh
+++ b/source/blender/blenkernel/BKE_screen.hh
@@ -11,6 +11,7 @@
 #include <string>
 
 #include "BLI_compiler_attrs.h"
+#include "BLI_math_vector_types.hh"
 #include "BLI_vector.hh"
 
 #include "RNA_types.hh"
@@ -295,6 +296,9 @@ struct PanelType {
   short region_type;
   /* For popovers, 0 for default. */
   int ui_units_x;
+  /** For popovers, position the popover at the given offset (multiplied by #UI_UNIT_X/#UI_UNIT_Y)
+   * relative to the top left corner, if it's not attached to a button. */
+  blender::float2 offset_units_xy;
   int order;
 
   int flag;
diff --git a/source/blender/editors/asset/CMakeLists.txt b/source/blender/editors/asset/CMakeLists.txt
index 3e387636b46..ecc1a6fd4c2 100644
--- a/source/blender/editors/asset/CMakeLists.txt
+++ b/source/blender/editors/asset/CMakeLists.txt
@@ -34,7 +34,7 @@ set(SRC
   intern/asset_shelf.cc
   intern/asset_shelf_asset_view.cc
   intern/asset_shelf_catalog_selector.cc
-  intern/asset_shelf_popup.cc
+  intern/asset_shelf_popover.cc
   intern/asset_shelf_regiondata.cc
   intern/asset_shelf_settings.cc
   intern/asset_temp_id_consumer.cc
diff --git a/source/blender/editors/asset/ED_asset_shelf.hh b/source/blender/editors/asset/ED_asset_shelf.hh
index f3ae9c8203b..5c99f6f979a 100644
--- a/source/blender/editors/asset/ED_asset_shelf.hh
+++ b/source/blender/editors/asset/ED_asset_shelf.hh
@@ -65,7 +65,7 @@ void header_region_init(wmWindowManager *wm, ARegion *region);
 void header_region(const bContext *C, ARegion *region);
 void header_region_listen(const wmRegionListenerParams *params);
 int header_region_size();
-void header_regiontype_register(ARegionType *region_type, const int space_type);
+void types_register(ARegionType *region_type, const int space_type);
 
 /** \} */
 
@@ -90,7 +90,6 @@ AssetShelfType *type_find_from_idname(const StringRef idname);
 /** \name Asset Shelf Popup
  * \{ */
 
-uiBlock *popup_block_create(const bContext *C, ARegion *region, AssetShelfType *shelf_type);
 void type_popup_unlink(const AssetShelfType &shelf_type);
 
 /** \} */
diff --git a/source/blender/editors/asset/intern/asset_shelf.cc b/source/blender/editors/asset/intern/asset_shelf.cc
index 788b2e41c7e..60b0ba01c06 100644
--- a/source/blender/editors/asset/intern/asset_shelf.cc
+++ b/source/blender/editors/asset/intern/asset_shelf.cc
@@ -13,6 +13,7 @@
 #include "AS_asset_catalog_path.hh"
 #include "AS_asset_library.hh"
 
+#include "BLI_function_ref.hh"
 #include "BLI_string.h"
 
 #include "BKE_context.hh"
@@ -831,7 +832,7 @@ static void asset_shelf_header_draw(const bContext *C, Header *header)
   uiItemR(sub, &shelf_ptr, "search_filter", UI_ITEM_NONE, "", ICON_VIEWZOOM);
 }
 
-void header_regiontype_register(ARegionType *region_type, const int space_type)
+static void header_regiontype_register(ARegionType *region_type, const int space_type)
 {
   HeaderType *ht = MEM_cnew<HeaderType>(__func__);
   STRNCPY(ht->idname, "ASSETSHELF_HT_settings");
@@ -843,8 +844,13 @@ void header_regiontype_register(ARegionType *region_type, const int space_type)
   };
 
   BLI_addtail(&region_type->headertypes, ht);
+}
 
+void types_register(ARegionType *region_type, const int space_type)
+{
+  header_regiontype_register(region_type, space_type);
   catalog_selector_panel_register(region_type);
+  popover_panel_register(region_type);
 }
 
 /** \} */
diff --git a/source/blender/editors/asset/intern/asset_shelf.hh b/source/blender/editors/asset/intern/asset_shelf.hh
index 9270d631861..261a5716c8f 100644
--- a/source/blender/editors/asset/intern/asset_shelf.hh
+++ b/source/blender/editors/asset/intern/asset_shelf.hh
@@ -38,6 +38,7 @@ void build_asset_view(uiLayout &layout,
                       const ARegion &region);
 
 void catalog_selector_panel_register(ARegionType *region_type);
+void popover_panel_register(ARegionType *region_type);
 
 AssetShelf *active_shelf_from_context(const bContext *C);
 
diff --git a/source/blender/editors/asset/intern/asset_shelf_asset_view.cc b/source/blender/editors/asset/intern/asset_shelf_asset_view.cc
index b92ee51aac8..2bc40461c3e 100644
--- a/source/blender/editors/asset/intern/asset_shelf_asset_view.cc
+++ b/source/blender/editors/asset/intern/asset_shelf_asset_view.cc
@@ -11,6 +11,7 @@
 #include "AS_asset_library.hh"
 #include "AS_asset_representation.hh"
 
+#include "BKE_asset.hh"
 #include "BKE_screen.hh"
 
 #include "BLI_fnmatch.h"
@@ -41,13 +42,12 @@ class AssetView : public ui::AbstractGridView {
   const AssetShelf &shelf_;
   std::optional<AssetWeakReference> active_asset_;
   std::optional<asset_system::AssetCatalogFilter> catalog_filter_ = std::nullopt;
-  bool is_popup_ = false;
 
   friend class AssetViewItem;
   friend class AssetDragController;
 
  public:
-  AssetView(const AssetLibraryReference &library_ref, const AssetShelf &shelf, bool is_popup);
+  AssetView(const AssetLibraryReference &library_ref, const AssetShelf &shelf);
 
   void build_items() override;
   bool begin_filtering(const bContext &C) const override;
@@ -84,10 +84,8 @@ class AssetDragController : public ui::AbstractViewItemDragController {
   void *create_drag_data() const override;
 };
 
-AssetView::AssetView(const AssetLibraryReference &library_ref,
-                     const AssetShelf &shelf,
-                     const bool is_popup)
-    : library_ref_(library_ref), shelf_(shelf), is_popup_(is_popup)
+AssetView::AssetView(const AssetLibraryReference &library_ref, const AssetShelf &shelf)
+    : library_ref_(library_ref), shelf_(shelf)
 {
   if (shelf.type->get_active_asset) {
     if (const AssetWeakReference *weak_ref = shelf.type->get_active_asset(shelf.type)) {
@@ -294,8 +292,7 @@ void build_asset_view(uiLayout &layout,
   BLI_assert(tile_width != 0);
   BLI_assert(tile_height != 0);
 
-  const bool is_popup = region.regiontype == RGN_TYPE_TEMPORARY;
-  std::unique_ptr asset_view = std::make_unique<AssetView>(library_ref, shelf, is_popup);
+  std::unique_ptr asset_view = std::make_unique<AssetView>(library_ref, shelf);
   asset_view->set_catalog_filter(catalog_filter_from_shelf_settings(shelf.settings, *library));
   asset_view->set_tile_size(tile_width, tile_height);
 
diff --git a/source/blender/editors/asset/intern/asset_shelf_popup.cc b/source/blender/editors/asset/intern/asset_shelf_popover.cc
similarity index 63%
rename from source/blender/editors/asset/intern/asset_shelf_popup.cc
rename to source/blender/editors/asset/intern/asset_shelf_popover.cc
index 99e729b3367..6aa08f29eab 100644
--- a/source/blender/editors/asset/intern/asset_shelf_popup.cc
+++ b/source/blender/editors/asset/intern/asset_shelf_popover.cc
@@ -10,6 +10,8 @@
 
 #include "BKE_screen.hh"
 
+#include "BLI_string.h"
+
 #include "BLT_translation.hh"
 
 #include "UI_interface_c.hh"
@@ -22,6 +24,8 @@
 #include "RNA_access.hh"
 #include "RNA_prototypes.h"
 
+#include "WM_api.hh"
+
 namespace blender::ed::asset::shelf {
 
 class StaticPopupShelves {
@@ -51,20 +55,20 @@ void type_popup_unlink(const AssetShelfType &shelf_type)
   }
 }
 
-static AssetShelf *get_shelf_for_popup(const bContext *C, AssetShelfType &shelf_type)
+static AssetShelf *get_shelf_for_popup(const bContext &C, AssetShelfType &shelf_type)
 {
   Vector<AssetShelf *> &popup_shelves = StaticPopupShelves::shelves();
 
   for (AssetShelf *shelf : popup_shelves) {
     if (STREQ(shelf->idname, shelf_type.idname)) {
-      if (type_poll_for_popup(*C, ensure_shelf_has_type(*shelf))) {
+      if (type_poll_for_popup(C, ensure_shelf_has_type(*shelf))) {
         return shelf;
       }
       break;
     }
   }
 
-  if (type_poll_for_popup(*C, &shelf_type)) {
+  if (type_poll_for_popup(C, &shelf_type)) {
     AssetShelf *new_shelf = create_shelf_from_type(shelf_type);
     new_shelf->settings.display_flag |= ASSETSHELF_SHOW_NAMES;
     popup_shelves.append(new_shelf);
@@ -134,10 +138,16 @@ class AssetCatalogTreeView : public ui::AbstractTreeView {
       return settings_is_active_catalog(shelf_.settings, catalog_path);
     });
 
-    catalog_item.foreach_child(
-        [&view_item, this](const asset_system::AssetCatalogTreeItem &child) {
-          build_catalog_items_recursive(view_item, child);
-        });
+    const int parent_count = view_item.count_parents() + 1;
+
+    catalog_item.foreach_child([&, this](const asset_system::AssetCatalogTreeItem &child) {
+      ui::BasicTreeViewItem &child_item = build_catalog_items_recursive(view_item, child);
+
+      /* Uncollapse to some level (gives quick acces, but don't let the tree get too big). */
+      if (parent_count < 3) {
+        child_item.uncollapse_by_default();
+      }
+    });
 
     return view_item;
   }
@@ -160,36 +170,43 @@ static void catalog_tree_draw(uiLayout &layout, AssetShelf &shelf)
   ui::TreeViewBuilder::build_tree_view(*tree_view, layout);
 }
 
-uiBlock *popup_block_create(const bContext *C, ARegion *region, AssetShelfType *shelf_type)
+static AssetShelfType *lookup_type_from_idname_in_context(const bContext *C)
 {
-  bScreen *screen = CTX_wm_screen(C);
-  uiBlock *block = UI_block_begin(C, region, "_popup", UI_EMBOSS);
-  UI_block_flag_enable(block, UI_BLOCK_KEEP_OPEN | UI_BLOCK_POPOVER);
-  UI_block_theme_style_set(block, UI_BLOCK_THEME_STYLE_POPUP);
-  UI_block_bounds_set_normal(block, 0.3f * U.widget_unit);
-  UI_block_direction_set(block, UI_DIR_DOWN);
+  const std::optional<StringRefNull> idname = CTX_data_string_get(C, "asset_shelf_idname");
+  if (!idname) {
+    return nullptr;
+  }
+  return type_find_from_idname(*idname);
+}
 
-  AssetShelf *shelf = get_shelf_for_popup(C, *shelf_type);
+constexpr int LEFT_COL_WIDTH_UNITS = 10;
+constexpr int RIGHT_COL_WIDTH_UNITS = 30;
+constexpr int LAYOUT_WIDTH_UNITS = LEFT_COL_WIDTH_UNITS + RIGHT_COL_WIDTH_UNITS;
+
+static void popover_panel_draw(const bContext *C, Panel *panel)
+{
+  AssetShelfType *shelf_type = lookup_type_from_idname_in_context(C);
+  BLI_assert_msg(shelf_type != nullptr, "couldn't find asset shelf type from context");
+
+  const ARegion *region = CTX_wm_region_popup(C) ? CTX_wm_region_popup(C) : CTX_wm_region(C);
+
+  uiLayout *layout = panel->layout;
+  uiLayoutSetUnitsX(layout, LAYOUT_WIDTH_UNITS);
+
+  AssetShelf *shelf = get_shelf_for_popup(*C, *shelf_type);
   if (!shelf) {
     BLI_assert_unreachable();
-    return block;
+    return;
   }
 
-  const uiStyle *style = UI_style_get_dpi();
-
-  const int layout_width = UI_UNIT_X * 40;
-  const int left_col_width = 10 * UI_UNIT_X;
-  const int right_col_width = layout_width - left_col_width;
-  uiLayout *layout = UI_block_layout(
-      block, UI_LAYOUT_VERTICAL, UI_LAYOUT_PANEL, 0, 0, layout_width, 0, 0, style);
-
+  bScreen *screen = CTX_wm_screen(C);
   PointerRNA library_ref_ptr = RNA_pointer_create(
       &screen->id, &RNA_AssetLibraryReference, &shelf->settings.asset_library_reference);
   uiLayoutSetContextPointer(layout, "asset_library_reference", &library_ref_ptr);
 
   uiLayout *row = uiLayoutRow(layout, false);
   uiLayout *catalogs_col = uiLayoutColumn(row, false);
-  uiLayoutSetUnitsX(catalogs_col, left_col_width / UI_UNIT_X);
+  uiLayoutSetUnitsX(catalogs_col, LEFT_COL_WIDTH_UNITS);
   uiLayoutSetFixedSize(catalogs_col, true);
   library_selector_draw(C, catalogs_col, *shelf);
   catalog_tree_draw(*catalogs_col, *shelf);
@@ -198,14 +215,53 @@ uiBlock *popup_block_create(const bContext *C, ARegion *region, AssetShelfType *
   uiLayout *sub = uiLayoutRow(right_col, false);
   /* Same as file/asset browser header. */
   PointerRNA shelf_ptr = RNA_pointer_create(&screen->id, &RNA_AssetShelf, shelf);
-  uiItemR(sub, &shelf_ptr, "search_filter", UI_ITEM_R_IMMEDIATE, "", ICON_VIEWZOOM);
+  uiItemR(sub,
+          &shelf_ptr,
+          "search_filter",
+          /* Force the button to be active in a semi-modal state. */
+          UI_ITEM_R_TEXT_BUT_FORCE_SEMI_MODAL_ACTIVE,
+          "",
+          ICON_VIEWZOOM);
 
   uiLayout *asset_view_col = uiLayoutColumn(right_col, false);
-  uiLayoutSetUnitsX(asset_view_col, right_col_width / UI_UNIT_X);
+  uiLayoutSetUnitsX(asset_view_col, RIGHT_COL_WIDTH_UNITS);
   uiLayoutSetFixedSize(asset_view_col, true);
-  build_asset_view(*asset_view_col, shelf->settings.asset_library_reference, *shelf, *C, *region);
 
-  return block;
+  build_asset_view(*asset_view_col, shelf->settings.asset_library_reference, *shelf, *C, *region);
+}
+
+static bool popover_panel_poll(const bContext *C, PanelType * /*panel_type*/)
+{
+  const AssetShelfType *shelf_type = lookup_type_from_idname_in_context(C);
+  if (!shelf_type) {
+    return false;
+  }
+
+  return type_poll_for_popup(*C, shelf_type);
+}
+
+void popover_panel_register(ARegionType *region_type)
+{
+  /* Uses global paneltype registry to allow usage as popover. So only register this once (may be
+   * called from multiple spaces). */
+  if (WM_paneltype_find("ASSETSHELF_PT_popover_panel", true)) {
+    return;
+  }
+
+  PanelType *pt = MEM_cnew<PanelType>(__func__);
+  STRNCPY(pt->idname, "ASSETSHELF_PT_popover_panel");
+  STRNCPY(pt->label, N_("Asset Shelf Panel"));
+  STRNCPY(pt->translation_context, BLT_I18NCONTEXT_DEFAULT_BPYRNA);
+  pt->description = N_("Display an asset shelf in a popover panel");
+  pt->draw = popover_panel_draw;
+  pt->poll = popover_panel_poll;
+  pt->listener = asset::list::asset_reading_region_listen_fn;
+  /* Move to have first asset item under cursor. */
+  pt->offset_units_xy.x = -(LEFT_COL_WIDTH_UNITS + 1.5f);
+  /* Offset so mouse is below search button, over the first row of assets. */
+  pt->offset_units_xy.y = 2.5f;
+  BLI_addtail(&region_type->paneltypes, pt);
+  WM_paneltype_add(pt);
 }
 
 }  // namespace blender::ed::asset::shelf
diff --git a/source/blender/editors/include/UI_interface.hh b/source/blender/editors/include/UI_interface.hh
index 4288fe0be90..9815f383c3b 100644
--- a/source/blender/editors/include/UI_interface.hh
+++ b/source/blender/editors/include/UI_interface.hh
@@ -91,6 +91,9 @@ void attribute_search_add_items(StringRefNull str,
                                 uiSearchItems *items,
                                 bool is_first);
 
+bool asset_shelf_popover_invoke(bContext &C,
+                                blender::StringRef asset_shelf_idname,
+                                ReportList &reports);
 /**
  * Some drop targets simply allow dropping onto/into them, others support dragging in-between them.
  * Classes implementing the drop-target interface can use this type to control the behavior by
diff --git a/source/blender/editors/include/UI_interface_c.hh b/source/blender/editors/include/UI_interface_c.hh
index 7130c73c9aa..c32feaeba6d 100644
--- a/source/blender/editors/include/UI_interface_c.hh
+++ b/source/blender/editors/include/UI_interface_c.hh
@@ -2269,6 +2269,10 @@ MenuType *UI_but_menutype_get(const uiBut *but);
  * This is a bit of a hack but best keep it in one place at least.
  */
 PanelType *UI_but_paneltype_get(const uiBut *but);
+/**
+ * This is a bit of a hack but best keep it in one place at least.
+ */
+std::optional<blender::StringRefNull> UI_but_asset_shelf_type_idname_get(const uiBut *but);
 void UI_menutype_draw(bContext *C, MenuType *mt, uiLayout *layout);
 /**
  * Used for popup panels only.
@@ -2789,8 +2793,11 @@ void uiTemplateAssetView(uiLayout *layout,
 
 namespace blender::ui {
 
-void template_asset_shelf_popover(
-    uiLayout &layout, const bContext &C, StringRefNull asset_shelf_id, StringRef name, int icon);
+void template_asset_shelf_popover(uiLayout &layout,
+                                  const bContext &C,
+                                  StringRefNull asset_shelf_id,
+                                  StringRefNull name,
+                                  int icon);
 
 }
 
diff --git a/source/blender/editors/interface/interface_context_menu.cc b/source/blender/editors/interface/interface_context_menu.cc
index 07a10906f8c..f688565e758 100644
--- a/source/blender/editors/interface/interface_context_menu.cc
+++ b/source/blender/editors/interface/interface_context_menu.cc
@@ -114,6 +114,13 @@ static const char *shortcut_get_operator_property(bContext *C, uiBut *but, IDPro
     return "WM_OT_call_menu";
   }
 
+  if (std::optional asset_shelf_idname = UI_but_asset_shelf_type_idname_get(but)) {
+    IDProperty *prop = blender::bke::idprop::create_group(__func__).release();
+    IDP_AddToGroup(prop, bke::idprop::create("name", *asset_shelf_idname).release());
+    *r_prop = prop;
+    return "WM_OT_call_asset_shelf_popover";
+  }
+
   if (PanelType *pt = UI_but_paneltype_get(but)) {
     IDProperty *prop = blender::bke::idprop::create_group(__func__).release();
     IDP_AddToGroup(prop, bke::idprop::create("name", pt->idname).release());
diff --git a/source/blender/editors/interface/interface_intern.hh b/source/blender/editors/interface/interface_intern.hh
index 6f6927e2fcf..68d5a806f70 100644
--- a/source/blender/editors/interface/interface_intern.hh
+++ b/source/blender/editors/interface/interface_intern.hh
@@ -1014,10 +1014,12 @@ uiPopupBlockHandle *ui_popup_menu_create(
 
 /* `interface_region_popover.cc` */
 
+using uiPopoverCreateFunc = std::function<void(bContext *, uiLayout *, PanelType *)>;
+
 uiPopupBlockHandle *ui_popover_panel_create(bContext *C,
                                             ARegion *butregion,
                                             uiBut *but,
-                                            uiMenuCreateFunc menu_func,
+                                            uiPopoverCreateFunc popover_func,
                                             const PanelType *panel_type);
 
 /* `interface_region_menu_pie.cc` */
@@ -1552,6 +1554,9 @@ void UI_OT_eyedropper_driver(wmOperatorType *ot);
 
 void UI_OT_eyedropper_gpencil_color(wmOperatorType *ot);
 
+/* interface_template_asset_shelf_popover.cc */
+std::optional<blender::StringRefNull> UI_asset_shelf_idname_from_button_context(const uiBut *but);
+
 /* interface_template_asset_view.cc */
 
 uiListType *UI_UL_asset_view();
diff --git a/source/blender/editors/interface/interface_layout.cc b/source/blender/editors/interface/interface_layout.cc
index 528157a5db0..da96fa3b402 100644
--- a/source/blender/editors/interface/interface_layout.cc
+++ b/source/blender/editors/interface/interface_layout.cc
@@ -3195,6 +3195,10 @@ void uiItemPopoverPanel_ptr(
     icon = ICON_BLANK1;
   }
 
+  const bContextStore *previous_ctx = CTX_store_get(C);
+  /* Set context for polling (and panel header drawing). */
+  CTX_store_set(const_cast<bContext *>(C), layout->context);
+
   const bool ok = (pt->poll == nullptr) || pt->poll(C, pt);
   if (ok && (pt->draw_header != nullptr)) {
     layout = uiLayoutRow(layout, true);
@@ -3206,6 +3210,9 @@ void uiItemPopoverPanel_ptr(
     panel.flag = PNL_POPOVER;
     pt->draw_header(C, &panel);
   }
+
+  CTX_store_set(const_cast<bContext *>(C), previous_ctx);
+
   uiBut *but = ui_item_menu(
       layout, name, icon, ui_item_paneltype_func, pt, nullptr, TIP_(pt->description), true);
   but->type = UI_BTYPE_POPOVER;
@@ -6109,6 +6116,11 @@ PanelType *UI_but_paneltype_get(const uiBut *but)
   return nullptr;
 }
 
+std::optional<blender::StringRefNull> UI_but_asset_shelf_type_idname_get(const uiBut *but)
+{
+  return UI_asset_shelf_idname_from_button_context(but);
+}
+
 void UI_menutype_draw(bContext *C, MenuType *mt, uiLayout *layout)
 {
   Menu menu{};
diff --git a/source/blender/editors/interface/regions/interface_region_popover.cc b/source/blender/editors/interface/regions/interface_region_popover.cc
index b9483ed6402..2bd6fd463da 100644
--- a/source/blender/editors/interface/regions/interface_region_popover.cc
+++ b/source/blender/editors/interface/regions/interface_region_popover.cc
@@ -61,8 +61,8 @@ struct uiPopover {
   wmKeyMap *keymap;
   wmEventHandler_Keymap *keymap_handler;
 
-  uiMenuCreateFunc menu_func;
-  const PanelType *menu_arg;
+  uiPopoverCreateFunc popover_func;
+  const PanelType *panel_type;
 
   /* Size in pixels (ui scale applied). */
   int ui_size_x;
@@ -114,9 +114,9 @@ static uiBlock *ui_block_func_POPOVER(bContext *C, uiPopupBlockHandle *handle, v
   if (!pup->layout) {
     ui_popover_create_block(C, handle->region, pup, WM_OP_INVOKE_REGION_WIN);
 
-    if (pup->menu_func) {
+    if (pup->popover_func) {
       pup->block->handle = handle;
-      pup->menu_func(C, pup->layout, const_cast<PanelType *>(pup->menu_arg));
+      pup->popover_func(C, pup->layout, const_cast<PanelType *>(pup->panel_type));
       pup->block->handle = nullptr;
     }
 
@@ -185,6 +185,20 @@ static uiBlock *ui_block_func_POPOVER(bContext *C, uiPopupBlockHandle *handle, v
      * areas near the bottom of the window on refreshes. */
     handle->max_size_y = UI_UNIT_Y * 16.0f;
   }
+  else if (pup->panel_type &&
+           (pup->panel_type->offset_units_xy.x || pup->panel_type->offset_units_xy.y))
+  {
+    UI_block_flag_enable(block, UI_BLOCK_LOOP);
+    UI_block_theme_style_set(block, UI_BLOCK_THEME_STYLE_POPUP);
+    UI_block_direction_set(block, block->direction);
+    block->minbounds = UI_MENU_WIDTH_MIN;
+
+    const int bounds_offset[2] = {
+        int(pup->panel_type->offset_units_xy.x * UI_UNIT_X),
+        int(pup->panel_type->offset_units_xy.y * UI_UNIT_Y),
+    };
+    UI_block_bounds_set_popup(block, block_margin, bounds_offset);
+  }
   else {
     /* Not attached to a button. */
     int bounds_offset[2] = {0, 0};
@@ -233,20 +247,20 @@ static void ui_block_free_func_POPOVER(void *arg_pup)
     wmWindow *window = pup->window;
     WM_event_remove_keymap_handler(&window->modalhandlers, pup->keymap);
   }
-  MEM_freeN(pup);
+  MEM_delete(pup);
 }
 
 uiPopupBlockHandle *ui_popover_panel_create(bContext *C,
                                             ARegion *butregion,
                                             uiBut *but,
-                                            uiMenuCreateFunc menu_func,
+                                            uiPopoverCreateFunc popover_func,
                                             const PanelType *panel_type)
 {
   wmWindow *window = CTX_wm_window(C);
   const uiStyle *style = UI_style_get_dpi();
 
   /* Create popover, buttons are created from callback. */
-  uiPopover *pup = MEM_cnew<uiPopover>(__func__);
+  uiPopover *pup = MEM_new<uiPopover>(__func__);
   pup->but = but;
 
   /* FIXME: maybe one day we want non panel popovers? */
@@ -259,8 +273,8 @@ uiPopupBlockHandle *ui_popover_panel_create(bContext *C,
                      (text_points_max / float(UI_DEFAULT_TEXT_POINTS));
   }
 
-  pup->menu_func = menu_func;
-  pup->menu_arg = panel_type;
+  pup->popover_func = popover_func;
+  pup->panel_type = panel_type;
 
 #ifdef USE_UI_POPOVER_ONCE
   {
@@ -335,7 +349,7 @@ int UI_popover_panel_invoke(bContext *C, const char *idname, bool keep_open, Rep
 
 uiPopover *UI_popover_begin(bContext *C, int ui_menu_width, bool from_active_button)
 {
-  uiPopover *pup = MEM_cnew<uiPopover>(__func__);
+  uiPopover *pup = MEM_new<uiPopover>(__func__);
   if (ui_menu_width == 0) {
     ui_menu_width = U.widget_unit * UI_POPOVER_WIDTH_UNITS;
   }
diff --git a/source/blender/editors/interface/templates/interface_template_asset_shelf_popover.cc b/source/blender/editors/interface/templates/interface_template_asset_shelf_popover.cc
index 421a5d00547..4ae4dfa369a 100644
--- a/source/blender/editors/interface/templates/interface_template_asset_shelf_popover.cc
+++ b/source/blender/editors/interface/templates/interface_template_asset_shelf_popover.cc
@@ -7,28 +7,28 @@
  */
 
 #include "BKE_context.hh"
+#include "BKE_report.hh"
 #include "BKE_screen.hh"
 
 #include "RNA_access.hh"
+#include "RNA_define.hh"
+#include "RNA_prototypes.h"
 
+#include "UI_interface.hh"
 #include "UI_interface_c.hh"
 #include "UI_resources.hh"
 #include "interface_intern.hh"
 
 #include "ED_asset_shelf.hh"
 
-namespace blender::ui {
+#include "WM_api.hh"
 
-static uiBlock *asset_shelf_block_fn(bContext *C, ARegion *region, void *arg_shelf_type)
-{
-  AssetShelfType *shelf_type = reinterpret_cast<AssetShelfType *>(arg_shelf_type);
-  return ed::asset::shelf::popup_block_create(C, region, shelf_type);
-}
+namespace blender::ui {
 
 void template_asset_shelf_popover(uiLayout &layout,
                                   const bContext &C,
                                   const StringRefNull asset_shelf_id,
-                                  const StringRef name,
+                                  const StringRefNull name,
                                   const BIFIconID icon)
 {
   AssetShelfType *shelf_type = ed::asset::shelf::type_find_from_idname(asset_shelf_id);
@@ -38,30 +38,64 @@ void template_asset_shelf_popover(uiLayout &layout,
   }
 
   const ARegion *region = CTX_wm_region(&C);
+  uiBlock *block = uiLayoutGetBlock(&layout);
+
+  uiLayout *row = uiLayoutRow(&layout, true);
   const bool use_big_size = !RGN_TYPE_IS_HEADER_ANY(region->regiontype);
   const bool use_preview_icon = use_big_size;
-  const short width = [&]() -> short {
-    if (use_big_size) {
-      return UI_UNIT_X * 6;
-    }
-    return UI_UNIT_X * (name.is_empty() ? 1.6f : 7);
-  }();
-  const short height = UI_UNIT_Y * (use_big_size ? 6 : 1);
 
-  uiBlock *block = uiLayoutGetBlock(&layout);
-  uiBut *but = uiDefBlockBut(
-      block, asset_shelf_block_fn, shelf_type, name, 0, 0, width, height, "Select an asset");
+  uiLayoutSetContextString(row, "asset_shelf_idname", asset_shelf_id);
+  if (use_big_size) {
+    uiLayoutSetScaleX(row, 6);
+    uiLayoutSetScaleY(row, 6);
+  }
+  else {
+    uiLayoutSetUnitsX(row, name.is_empty() ? 1.6f : 7);
+  }
+
+  uiItemPopoverPanel(row, &C, "ASSETSHELF_PT_popover_panel", name.c_str(), icon);
+  uiBut *but = static_cast<uiBut *>(block->buttons.last);
   if (use_preview_icon) {
     ui_def_but_icon(but, icon, UI_HAS_ICON | UI_BUT_ICON_PREVIEW);
   }
-  else {
-    ui_def_but_icon(but, icon, UI_HAS_ICON);
-    UI_but_drawflag_enable(but, UI_BUT_ICON_LEFT);
+}
+
+bool asset_shelf_popover_invoke(bContext &C, StringRef asset_shelf_idname, ReportList &reports)
+{
+  AssetShelfType *shelf_type = ed::asset::shelf::type_find_from_idname(asset_shelf_idname);
+  if (ed::asset::shelf::type_poll_for_popup(C, shelf_type) == false) {
+    return false;
   }
 
-  if (ed::asset::shelf::type_poll_for_popup(C, shelf_type) == false) {
-    UI_but_flag_enable(but, UI_BUT_DISABLED);
+  PanelType *pt = WM_paneltype_find("ASSETSHELF_PT_popover_panel", true);
+  if (pt == nullptr) {
+    BKE_reportf(&reports, RPT_ERROR, "Asset shelf popover panel type not found");
+    return false;
   }
+
+  /* Skip panel poll check here. Should usually be done, but requires passing the asset shelf type
+   * name via some context-store, but there's nothing to provide that here. Asset shelf type is
+   * polled above, so it's okay. */
+
+  std::string asset_shelf_id_str = asset_shelf_idname;
+  ui_popover_panel_create(
+      &C,
+      nullptr,
+      nullptr,
+      [asset_shelf_id_str](bContext *C, uiLayout *layout, void *arg_pt) {
+        uiLayoutSetContextString(layout, "asset_shelf_idname", asset_shelf_id_str);
+        ui_item_paneltype_func(C, layout, arg_pt);
+      },
+      pt);
+
+  return true;
 }
 
 }  // namespace blender::ui
+
+using namespace blender;
+
+std::optional<StringRefNull> UI_asset_shelf_idname_from_button_context(const uiBut *but)
+{
+  return UI_but_context_string_get(but, "asset_shelf_idname");
+}
diff --git a/source/blender/editors/space_image/space_image.cc b/source/blender/editors/space_image/space_image.cc
index e8234cb8a53..513790e5bd0 100644
--- a/source/blender/editors/space_image/space_image.cc
+++ b/source/blender/editors/space_image/space_image.cc
@@ -1224,7 +1224,7 @@ void ED_spacetype_image()
   art->listener = asset::shelf::header_region_listen;
   art->context = asset::shelf::context;
   BLI_addhead(&st->regiontypes, art);
-  asset::shelf::header_regiontype_register(art, SPACE_IMAGE);
+  asset::shelf::types_register(art, SPACE_IMAGE);
 
   /* regions: hud */
   art = ED_area_type_hud(st->spaceid);
diff --git a/source/blender/editors/space_view3d/space_view3d.cc b/source/blender/editors/space_view3d/space_view3d.cc
index 9dad3485753..386e6a98a99 100644
--- a/source/blender/editors/space_view3d/space_view3d.cc
+++ b/source/blender/editors/space_view3d/space_view3d.cc
@@ -2199,7 +2199,7 @@ void ED_spacetype_view3d()
   art->listener = asset::shelf::header_region_listen;
   art->context = asset::shelf::context;
   BLI_addhead(&st->regiontypes, art);
-  asset::shelf::header_regiontype_register(art, SPACE_VIEW3D);
+  asset::shelf::types_register(art, SPACE_VIEW3D);
 
   /* regions: hud */
   art = ED_area_type_hud(st->spaceid);
diff --git a/source/blender/makesrna/intern/rna_ui_api.cc b/source/blender/makesrna/intern/rna_ui_api.cc
index bea5d5ee2c5..0ca2e26b127 100644
--- a/source/blender/makesrna/intern/rna_ui_api.cc
+++ b/source/blender/makesrna/intern/rna_ui_api.cc
@@ -973,7 +973,7 @@ void rna_uiTemplateAssetShelfPopover(uiLayout *layout,
     icon = icon_value;
   }
 
-  blender::ui::template_asset_shelf_popover(*layout, *C, asset_shelf_id, name, icon);
+  blender::ui::template_asset_shelf_popover(*layout, *C, asset_shelf_id, name ? name : "", icon);
 }
 
 PointerRNA rna_uiTemplatePopupConfirm(uiLayout *layout,
diff --git a/source/blender/windowmanager/intern/wm_operators.cc b/source/blender/windowmanager/intern/wm_operators.cc
index 728cba0030f..fefe740ecf8 100644
--- a/source/blender/windowmanager/intern/wm_operators.cc
+++ b/source/blender/windowmanager/intern/wm_operators.cc
@@ -2254,6 +2254,39 @@ static void WM_OT_call_panel(wmOperatorType *ot)
   RNA_def_property_flag(prop, PROP_SKIP_SAVE);
 }
 
+static int asset_shelf_popover_invoke(bContext *C, wmOperator *op, const wmEvent * /*event*/)
+{
+  char *asset_shelf_id = RNA_string_get_alloc(op->ptr, "name", nullptr, 0, nullptr);
+  BLI_SCOPED_DEFER([&]() { MEM_freeN(asset_shelf_id); });
+
+  if (!blender::ui::asset_shelf_popover_invoke(*C, asset_shelf_id, *op->reports)) {
+    return OPERATOR_CANCELLED | OPERATOR_PASS_THROUGH;
+  }
+
+  return OPERATOR_INTERFACE;
+}
+
+/* Needs to be defined at WM level to be globally accessible. */
+static void WM_OT_call_asset_shelf_popover(wmOperatorType *ot)
+{
+  /* identifiers */
+  ot->name = "Call Asset Shelf Popover";
+  ot->idname = "WM_OT_call_asset_shelf_popover";
+  ot->description = "Open a predefined asset shelf in a popup";
+
+  /* api callbacks */
+  ot->invoke = asset_shelf_popover_invoke;
+
+  ot->flag = OPTYPE_INTERNAL;
+
+  RNA_def_string(ot->srna,
+                 "name",
+                 nullptr,
+                 0,
+                 "Asset Shelf Name",
+                 "Identifier of the asset shelf to display");
+}
+
 /** \} */
 
 /* -------------------------------------------------------------------- */
@@ -4140,6 +4173,7 @@ void wm_operatortypes_register()
   WM_operatortype_append(WM_OT_call_menu);
   WM_operatortype_append(WM_OT_call_menu_pie);
   WM_operatortype_append(WM_OT_call_panel);
+  WM_operatortype_append(WM_OT_call_asset_shelf_popover);
   WM_operatortype_append(WM_OT_radial_control);
   WM_operatortype_append(WM_OT_stereo3d_set);
 #if defined(WIN32)