diff --git a/source/blender/editors/asset/CMakeLists.txt b/source/blender/editors/asset/CMakeLists.txt
index 1ad84a1c0d2..3e387636b46 100644
--- a/source/blender/editors/asset/CMakeLists.txt
+++ b/source/blender/editors/asset/CMakeLists.txt
@@ -34,6 +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_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 a9a3751d0a6..0c4d8817197 100644
--- a/source/blender/editors/asset/ED_asset_shelf.hh
+++ b/source/blender/editors/asset/ED_asset_shelf.hh
@@ -21,6 +21,7 @@ struct BlendDataReader;
 struct BlendWriter;
 struct Main;
 struct SpaceType;
+struct uiBlock;
 struct RegionPollParams;
 struct wmWindowManager;
 
@@ -73,15 +74,25 @@ void header_regiontype_register(ARegionType *region_type, const int space_type);
 void type_register(std::unique_ptr<AssetShelfType> type);
 void type_unregister(const AssetShelfType &shelf_type);
 /**
- * Poll an asset shelf type for display as a permanent region in a space of a given type (the
- * type's #bl_space_type).
+ * Poll an asset shelf type for display as a popup. Doesn't check for space-type (the type's
+ * #bl_space_type) since popups should ignore this to allow displaying in any space.
+ *
+ * Permanent/non-popup asset shelf regions should use #type_poll_for_space_type() instead.
  */
-bool type_poll(const bContext &C, const AssetShelfType *shelf_type, const int space_type);
-
+bool type_poll_for_popup(const bContext &C, const AssetShelfType *shelf_type);
 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);
+
+/** \} */
+
 /* -------------------------------------------------------------------- */
 
 void type_unlink(const Main &bmain, 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 685e1b85f84..b95dd3b477c 100644
--- a/source/blender/editors/asset/intern/asset_shelf.cc
+++ b/source/blender/editors/asset/intern/asset_shelf.cc
@@ -76,14 +76,11 @@ void type_unregister(const AssetShelfType &shelf_type)
   shelf_types.remove(it - shelf_types.begin());
 }
 
-bool type_poll(const bContext &C, const AssetShelfType *shelf_type, const int space_type)
+static bool type_poll_no_spacetype_check(const bContext &C, const AssetShelfType *shelf_type)
 {
   if (!shelf_type) {
     return false;
   }
-  if (shelf_type->space_type && (space_type != shelf_type->space_type)) {
-    return false;
-  }
 
 #ifndef NDEBUG
   const Vector<std::unique_ptr<AssetShelfType>> &shelf_types = static_shelf_types();
@@ -98,6 +95,31 @@ bool type_poll(const bContext &C, const AssetShelfType *shelf_type, const int sp
   return !shelf_type->poll || shelf_type->poll(&C, shelf_type);
 }
 
+bool type_poll_for_popup(const bContext &C, const AssetShelfType *shelf_type)
+{
+  return type_poll_no_spacetype_check(C, shelf_type);
+}
+
+/**
+ * Poll an asset shelf type for display as a permanent region in a space of a given type (the
+ * type's #bl_space_type).
+ *
+ * Popup asset shelves should use #type_poll_for_popup() instead.
+ */
+static bool type_poll_for_non_popup(const bContext &C,
+                                    const AssetShelfType *shelf_type,
+                                    const int space_type)
+{
+  if (!shelf_type) {
+    return false;
+  }
+  if (shelf_type->space_type && (space_type != shelf_type->space_type)) {
+    return false;
+  }
+
+  return type_poll_no_spacetype_check(C, shelf_type);
+}
+
 AssetShelfType *type_find_from_idname(const StringRef idname)
 {
   for (const std::unique_ptr<AssetShelfType> &shelf_type : static_shelf_types()) {
@@ -186,7 +208,8 @@ static AssetShelf *update_active_shelf(const bContext &C,
 
   /* Case 1: */
   if (shelf_regiondata.active_shelf &&
-      type_poll(C, ensure_shelf_has_type(*shelf_regiondata.active_shelf), space_type))
+      type_poll_for_non_popup(
+          C, ensure_shelf_has_type(*shelf_regiondata.active_shelf), space_type))
   {
     /* Not a strong precondition, but if this is wrong something weird might be going on. */
     BLI_assert(shelf_regiondata.active_shelf == shelf_regiondata.shelves.first);
@@ -200,7 +223,7 @@ static AssetShelf *update_active_shelf(const bContext &C,
       continue;
     }
 
-    if (type_poll(C, ensure_shelf_has_type(*shelf), space_type)) {
+    if (type_poll_for_non_popup(C, ensure_shelf_has_type(*shelf), space_type)) {
       /* Found a valid previously activated shelf, reactivate it. */
       activate_shelf(shelf_regiondata, *shelf);
       return shelf;
@@ -209,7 +232,7 @@ static AssetShelf *update_active_shelf(const bContext &C,
 
   /* Case 3: */
   for (const std::unique_ptr<AssetShelfType> &shelf_type : static_shelf_types()) {
-    if (type_poll(C, shelf_type.get(), space_type)) {
+    if (type_poll_for_non_popup(C, shelf_type.get(), space_type)) {
       AssetShelf *new_shelf = create_shelf_from_type(*shelf_type);
       BLI_addhead(&shelf_regiondata.shelves, new_shelf);
       /* Moves ownership to the regiondata. */
@@ -258,7 +281,7 @@ static bool asset_shelf_space_poll(const bContext *C, const SpaceLink *space_lin
 {
   /* Is there any asset shelf type registered that returns true for it's poll? */
   for (const std::unique_ptr<AssetShelfType> &shelf_type : static_shelf_types()) {
-    if (type_poll(*C, shelf_type.get(), space_link->spacetype)) {
+    if (type_poll_for_non_popup(*C, shelf_type.get(), space_link->spacetype)) {
       return true;
     }
   }
@@ -842,6 +865,8 @@ void type_unlink(const Main &bmain, const AssetShelfType &shelf_type)
       }
     }
   }
+
+  type_popup_unlink(shelf_type);
 }
 
 /** \} */
diff --git a/source/blender/editors/asset/intern/asset_shelf.hh b/source/blender/editors/asset/intern/asset_shelf.hh
index 234e345ad55..9270d631861 100644
--- a/source/blender/editors/asset/intern/asset_shelf.hh
+++ b/source/blender/editors/asset/intern/asset_shelf.hh
@@ -46,6 +46,8 @@ void send_redraw_notifier(const bContext &C);
 AssetShelfType *ensure_shelf_has_type(AssetShelf &shelf);
 AssetShelf *create_shelf_from_type(AssetShelfType &type);
 
+void library_selector_draw(const bContext *C, uiLayout *layout, AssetShelf &shelf);
+
 /**
  * Deep-copies \a shelf_regiondata into newly allocated memory. Must be freed using
  * #regiondata_free().
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 34599b015d9..7536fb9a7bb 100644
--- a/source/blender/editors/asset/intern/asset_shelf_asset_view.cc
+++ b/source/blender/editors/asset/intern/asset_shelf_asset_view.cc
@@ -44,12 +44,13 @@ class AssetView : public ui::AbstractGridView {
    * end of the string, for `fnmatch()` to work. */
   char search_string[sizeof(AssetShelfSettings::search_string) + 2] = "";
   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);
+  AssetView(const AssetLibraryReference &library_ref, const AssetShelf &shelf, bool is_popup);
 
   void build_items() override;
   bool begin_filtering(const bContext &C) const override;
@@ -70,6 +71,7 @@ class AssetViewItem : public ui::PreviewGridItem {
   void disable_asset_drag();
   void build_grid_tile(uiLayout &layout) const override;
   void build_context_menu(bContext &C, uiLayout &column) const override;
+  void on_activate(bContext &C) override;
   std::optional<bool> should_be_active() const override;
   bool is_filtered_visible() const override;
 
@@ -86,8 +88,10 @@ class AssetDragController : public ui::AbstractViewItemDragController {
   void *create_drag_data() const override;
 };
 
-AssetView::AssetView(const AssetLibraryReference &library_ref, const AssetShelf &shelf)
-    : library_ref_(library_ref), shelf_(shelf)
+AssetView::AssetView(const AssetLibraryReference &library_ref,
+                     const AssetShelf &shelf,
+                     const bool is_popup)
+    : library_ref_(library_ref), shelf_(shelf), is_popup_(is_popup)
 {
   if (shelf.settings.search_string[0]) {
     BLI_strncpy_ensure_pad(
@@ -236,6 +240,14 @@ void AssetViewItem::build_context_menu(bContext &C, uiLayout &column) const
   }
 }
 
+void AssetViewItem::on_activate(bContext & /*C*/)
+{
+  const AssetView &asset_view = dynamic_cast<const AssetView &>(this->get_view());
+  if (asset_view.is_popup_) {
+    UI_popup_menu_close_from_but(reinterpret_cast<uiBut *>(this->view_item_button()));
+  }
+}
+
 std::optional<bool> AssetViewItem::should_be_active() const
 {
   const AssetView &asset_view = dynamic_cast<const AssetView &>(this->get_view());
@@ -290,7 +302,8 @@ void build_asset_view(uiLayout &layout,
   BLI_assert(tile_width != 0);
   BLI_assert(tile_height != 0);
 
-  std::unique_ptr asset_view = std::make_unique<AssetView>(library_ref, shelf);
+  const bool is_popup = region.regiontype == RGN_TYPE_TEMPORARY;
+  std::unique_ptr asset_view = std::make_unique<AssetView>(library_ref, shelf, is_popup);
   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_catalog_selector.cc b/source/blender/editors/asset/intern/asset_shelf_catalog_selector.cc
index 9446f75cb2e..4a9c4c6e60a 100644
--- a/source/blender/editors/asset/intern/asset_shelf_catalog_selector.cc
+++ b/source/blender/editors/asset/intern/asset_shelf_catalog_selector.cc
@@ -174,32 +174,37 @@ void AssetCatalogSelectorTree::update_shelf_settings_from_enabled_catalogs()
   });
 }
 
+void library_selector_draw(const bContext *C, uiLayout *layout, AssetShelf &shelf)
+{
+  uiLayoutSetOperatorContext(layout, WM_OP_INVOKE_DEFAULT);
+
+  PointerRNA shelf_ptr = RNA_pointer_create(&CTX_wm_screen(C)->id, &RNA_AssetShelf, &shelf);
+
+  uiLayout *row = uiLayoutRow(layout, true);
+  uiItemR(row, &shelf_ptr, "asset_library_reference", UI_ITEM_NONE, "", ICON_NONE);
+  if (shelf.settings.asset_library_reference.type != ASSET_LIBRARY_LOCAL) {
+    uiItemO(row, "", ICON_FILE_REFRESH, "ASSET_OT_library_refresh");
+  }
+}
+
 static void catalog_selector_panel_draw(const bContext *C, Panel *panel)
 {
-  const AssetLibraryReference *library_ref = CTX_wm_asset_library_ref(C);
   AssetShelf *shelf = active_shelf_from_context(C);
   if (!shelf) {
     return;
   }
 
   uiLayout *layout = panel->layout;
-  uiBlock *block = uiLayoutGetBlock(layout);
 
-  uiLayoutSetOperatorContext(layout, WM_OP_INVOKE_DEFAULT);
+  library_selector_draw(C, layout, *shelf);
 
-  PointerRNA shelf_ptr = RNA_pointer_create(&CTX_wm_screen(C)->id, &RNA_AssetShelf, shelf);
-
-  uiLayout *row = uiLayoutRow(layout, true);
-  uiItemR(row, &shelf_ptr, "asset_library_reference", UI_ITEM_NONE, "", ICON_NONE);
-  if (library_ref->type != ASSET_LIBRARY_LOCAL) {
-    uiItemO(row, "", ICON_FILE_REFRESH, "ASSET_OT_library_refresh");
-  }
-
-  asset_system::AssetLibrary *library = list::library_get_once_available(*library_ref);
+  asset_system::AssetLibrary *library = list::library_get_once_available(
+      shelf->settings.asset_library_reference);
   if (!library) {
     return;
   }
 
+  uiBlock *block = uiLayoutGetBlock(layout);
   ui::AbstractTreeView *tree_view = UI_block_add_view(
       *block,
       "asset catalog tree view",
diff --git a/source/blender/editors/asset/intern/asset_shelf_popup.cc b/source/blender/editors/asset/intern/asset_shelf_popup.cc
new file mode 100644
index 00000000000..c4c989a4a4e
--- /dev/null
+++ b/source/blender/editors/asset/intern/asset_shelf_popup.cc
@@ -0,0 +1,208 @@
+/* SPDX-FileCopyrightText: 2024 Blender Authors
+ *
+ * SPDX-License-Identifier: GPL-2.0-or-later */
+
+/** \file
+ * \ingroup edasset
+ */
+
+#include "asset_shelf.hh"
+
+#include "BKE_screen.hh"
+
+#include "BLT_translation.hh"
+
+#include "UI_interface_c.hh"
+#include "UI_tree_view.hh"
+
+#include "ED_asset_filter.hh"
+#include "ED_asset_list.hh"
+#include "ED_asset_shelf.hh"
+
+#include "RNA_access.hh"
+#include "RNA_prototypes.h"
+
+namespace blender::ed::asset::shelf {
+
+class StaticPopupShelves {
+ public:
+  Vector<AssetShelf *> popup_shelves;
+
+  ~StaticPopupShelves()
+  {
+    for (AssetShelf *shelf : popup_shelves) {
+      MEM_delete(shelf);
+    }
+  }
+
+  static Vector<AssetShelf *> &shelves()
+  {
+    static StaticPopupShelves storage;
+    return storage.popup_shelves;
+  }
+};
+
+void type_popup_unlink(const AssetShelfType &shelf_type)
+{
+  for (AssetShelf *shelf : StaticPopupShelves::shelves()) {
+    if (shelf->type == &shelf_type) {
+      shelf->type = nullptr;
+    }
+  }
+}
+
+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))) {
+        return shelf;
+      }
+      break;
+    }
+  }
+
+  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);
+    return new_shelf;
+  }
+
+  return nullptr;
+}
+
+class AssetCatalogTreeView : public ui::AbstractTreeView {
+  AssetShelf &shelf_;
+  asset_system::AssetCatalogTree catalog_tree_;
+
+ public:
+  AssetCatalogTreeView(const asset_system::AssetLibrary &library, AssetShelf &shelf)
+      : shelf_(shelf)
+  {
+    catalog_tree_ = build_filtered_catalog_tree(
+        library,
+        shelf_.settings.asset_library_reference,
+        [this](const asset_system::AssetRepresentation &asset) {
+          return (!shelf_.type->asset_poll || shelf_.type->asset_poll(shelf_.type, &asset));
+        });
+  }
+
+  void build_tree() override
+  {
+    if (catalog_tree_.is_empty()) {
+      auto &item = this->add_tree_item<ui::BasicTreeViewItem>(RPT_("No applicable assets found"),
+                                                              ICON_INFO);
+      item.disable_interaction();
+      return;
+    }
+
+    auto &all_item = this->add_tree_item<ui::BasicTreeViewItem>(IFACE_("All"));
+    all_item.set_on_activate_fn([this](bContext &C, ui::BasicTreeViewItem &) {
+      settings_set_all_catalog_active(shelf_.settings);
+      send_redraw_notifier(C);
+    });
+    all_item.set_is_active_fn(
+        [this]() { return settings_is_all_catalog_active(shelf_.settings); });
+    all_item.uncollapse_by_default();
+
+    catalog_tree_.foreach_root_item([&, this](
+                                        const asset_system::AssetCatalogTreeItem &catalog_item) {
+      ui::BasicTreeViewItem &item = this->build_catalog_items_recursive(all_item, catalog_item);
+      item.uncollapse_by_default();
+    });
+  }
+
+  ui::BasicTreeViewItem &build_catalog_items_recursive(
+      ui::TreeViewOrItem &parent_view_item,
+      const asset_system::AssetCatalogTreeItem &catalog_item) const
+  {
+    ui::BasicTreeViewItem &view_item = parent_view_item.add_tree_item<ui::BasicTreeViewItem>(
+        catalog_item.get_name());
+
+    std::string catalog_path = catalog_item.catalog_path().str();
+    view_item.set_on_activate_fn([this, catalog_path](bContext &C, ui::BasicTreeViewItem &) {
+      settings_set_active_catalog(shelf_.settings, catalog_path);
+      send_redraw_notifier(C);
+    });
+    view_item.set_is_active_fn([this, catalog_path]() {
+      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);
+        });
+
+    return view_item;
+  }
+};
+
+static void catalog_tree_draw(uiLayout &layout, AssetShelf &shelf)
+{
+  const asset_system::AssetLibrary *library = list::library_get_once_available(
+      shelf.settings.asset_library_reference);
+  if (!library) {
+    return;
+  }
+
+  uiBlock *block = uiLayoutGetBlock(&layout);
+  ui::AbstractTreeView *tree_view = UI_block_add_view(
+      *block,
+      "asset shelf catalog tree view",
+      std::make_unique<AssetCatalogTreeView>(*library, shelf));
+
+  ui::TreeViewBuilder::build_tree_view(*tree_view, layout);
+}
+
+uiBlock *popup_block_create(const bContext *C, ARegion *region, AssetShelfType *shelf_type)
+{
+  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);
+
+  AssetShelf *shelf = get_shelf_for_popup(C, *shelf_type);
+  if (!shelf) {
+    BLI_assert_unreachable();
+    return block;
+  }
+
+  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);
+
+  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);
+  uiLayoutSetFixedSize(catalogs_col, true);
+  library_selector_draw(C, catalogs_col, *shelf);
+  catalog_tree_draw(*catalogs_col, *shelf);
+
+  uiLayout *right_col = uiLayoutColumn(row, false);
+  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);
+
+  uiLayout *asset_view_col = uiLayoutColumn(right_col, false);
+  uiLayoutSetUnitsX(asset_view_col, right_col_width / UI_UNIT_X);
+  uiLayoutSetFixedSize(asset_view_col, true);
+  build_asset_view(*asset_view_col, shelf->settings.asset_library_reference, *shelf, *C, *region);
+
+  return block;
+}
+
+}  // namespace blender::ed::asset::shelf
diff --git a/source/blender/editors/include/UI_interface_c.hh b/source/blender/editors/include/UI_interface_c.hh
index e09d38f0ee7..7d9bc98d949 100644
--- a/source/blender/editors/include/UI_interface_c.hh
+++ b/source/blender/editors/include/UI_interface_c.hh
@@ -710,6 +710,18 @@ uiLayout *UI_popup_menu_layout(uiPopupMenu *pup);
 void UI_popup_menu_reports(bContext *C, ReportList *reports) ATTR_NONNULL();
 int UI_popup_menu_invoke(bContext *C, const char *idname, ReportList *reports) ATTR_NONNULL(1, 2);
 
+/**
+ * If \a block is displayed in a popup menu, tag it for closing.
+ * \param is_cancel: If set to true, the popup will be closed as being cancelled (e.g. when
+ *                   pressing escape) as opposed to being handled successfully.
+ */
+void UI_popup_menu_close(const uiBlock *block, bool is_cancel = false);
+/**
+ * Version of #UI_popup_menu_close() that can be called on a button contained in a popup menu
+ * block. Convenience since the block may not be available.
+ */
+void UI_popup_menu_close_from_but(const uiBut *but, bool is_cancel = false);
+
 /**
  * Allow setting menu return value from externals.
  * E.g. WM might need to do this for exiting files correctly.
@@ -1496,6 +1508,10 @@ uiBut *uiDefIconMenuBut(uiBlock *block,
                         short height,
                         const char *tip);
 
+/**
+ * Note that \a fun can set the #UI_BLOCK_KEEP_OPEN flag to the block it creates, to allow
+ * refreshing the popup. That is, redrawing the layout, potentially affecting the popup size.
+ */
 uiBut *uiDefBlockBut(uiBlock *block,
                      uiBlockCreateFunc func,
                      void *arg,
@@ -2711,6 +2727,13 @@ void uiTemplateAssetView(uiLayout *layout,
                          const char *drag_opname,
                          PointerRNA *r_drag_op_properties);
 
+namespace blender::ui {
+
+void template_asset_shelf_popover(
+    uiLayout &layout, const bContext &C, StringRefNull asset_shelf_id, StringRef name, int icon);
+
+}
+
 void uiTemplateLightLinkingCollection(uiLayout *layout,
                                       uiLayout *context_layout,
                                       PointerRNA *ptr,
diff --git a/source/blender/editors/interface/CMakeLists.txt b/source/blender/editors/interface/CMakeLists.txt
index b7184589fdf..ecdb3ff924a 100644
--- a/source/blender/editors/interface/CMakeLists.txt
+++ b/source/blender/editors/interface/CMakeLists.txt
@@ -5,6 +5,7 @@
 set(INC
   .
   ../include
+  ../asset
   ../../asset_system
   ../../blenkernel
   ../../blenloader
@@ -64,6 +65,7 @@ set(SRC
   regions/interface_regions.cc
   interface_string_search.cc
   interface_style.cc
+  templates/interface_template_asset_shelf_popover.cc
   templates/interface_template_asset_view.cc
   templates/interface_template_attribute_search.cc
   templates/interface_template_bone_collection_tree.cc
diff --git a/source/blender/editors/interface/interface_handlers.cc b/source/blender/editors/interface/interface_handlers.cc
index 275618577b6..9d2fb624998 100644
--- a/source/blender/editors/interface/interface_handlers.cc
+++ b/source/blender/editors/interface/interface_handlers.cc
@@ -4048,6 +4048,8 @@ static void ui_do_but_textedit(
 
   if (changed || (retval == WM_UI_HANDLER_BREAK)) {
     ED_region_tag_redraw(data->region);
+    /* In case of popup regions, tag for popup refreshing too (contents may have changed). */
+    ED_region_tag_refresh_ui(data->region);
   }
 }
 
@@ -11509,6 +11511,8 @@ static int ui_handle_menus_recursive(bContext *C,
   if (!menu->retvalue) {
     ui_handle_viewlist_items_hover(event, menu->region);
   }
+  /* Handle mouse clicks on overlapping view item button. */
+  ui_handle_view_item_event(C, event, but, menu->region);
 
   if (do_towards_reinit) {
     ui_mouse_motion_towards_reinit(menu, event->xy);
diff --git a/source/blender/editors/interface/interface_intern.hh b/source/blender/editors/interface/interface_intern.hh
index 846b1b68619..1c8baabdbf2 100644
--- a/source/blender/editors/interface/interface_intern.hh
+++ b/source/blender/editors/interface/interface_intern.hh
@@ -984,6 +984,10 @@ uiBlock *ui_popup_block_refresh(bContext *C,
                                 ARegion *butregion,
                                 uiBut *but);
 
+/**
+ * Note that callbacks can set the #UI_BLOCK_KEEP_OPEN flag to the block it creates, to allow
+ * refreshing the popup. That is, redrawing the layout, potentially affecting the popup size.
+ */
 uiPopupBlockHandle *ui_popup_block_create(bContext *C,
                                           ARegion *butregion,
                                           uiBut *but,
diff --git a/source/blender/editors/interface/regions/interface_region_menu_popup.cc b/source/blender/editors/interface/regions/interface_region_menu_popup.cc
index 9e1a658fc0f..8cb725f8a51 100644
--- a/source/blender/editors/interface/regions/interface_region_menu_popup.cc
+++ b/source/blender/editors/interface/regions/interface_region_menu_popup.cc
@@ -765,4 +765,14 @@ bool UI_popup_block_name_exists(const bScreen *screen, const blender::StringRef
   return false;
 }
 
+void UI_popup_menu_close(const uiBlock *block, const bool is_cancel)
+{
+  UI_popup_menu_retval_set(block, is_cancel ? UI_RETURN_CANCEL : UI_RETURN_OK, true);
+}
+
+void UI_popup_menu_close_from_but(const uiBut *but, const bool is_cancel)
+{
+  UI_popup_menu_close(but->block, is_cancel);
+}
+
 /** \} */
diff --git a/source/blender/editors/interface/regions/interface_region_popup.cc b/source/blender/editors/interface/regions/interface_region_popup.cc
index f917e5c4e8d..10d2cba13e7 100644
--- a/source/blender/editors/interface/regions/interface_region_popup.cc
+++ b/source/blender/editors/interface/regions/interface_region_popup.cc
@@ -926,6 +926,10 @@ uiPopupBlockHandle *ui_popup_block_create(bContext *C,
     CTX_wm_region_popup_set(C, region_popup_prev);
   }
 
+  if (block->flag & UI_BLOCK_KEEP_OPEN) {
+    handle->can_refresh = true;
+  }
+
   /* keep centered on window resizing */
   if (block->bounds_type == UI_BLOCK_BOUNDS_POPUP_CENTER) {
     type.listener = ui_block_region_popup_window_listener;
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
new file mode 100644
index 00000000000..421a5d00547
--- /dev/null
+++ b/source/blender/editors/interface/templates/interface_template_asset_shelf_popover.cc
@@ -0,0 +1,67 @@
+/* SPDX-FileCopyrightText: 2024 Blender Authors
+ *
+ * SPDX-License-Identifier: GPL-2.0-or-later */
+
+/** \file
+ * \ingroup edinterface
+ */
+
+#include "BKE_context.hh"
+#include "BKE_screen.hh"
+
+#include "RNA_access.hh"
+
+#include "UI_interface_c.hh"
+#include "UI_resources.hh"
+#include "interface_intern.hh"
+
+#include "ED_asset_shelf.hh"
+
+namespace blender::ui {
+
+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);
+}
+
+void template_asset_shelf_popover(uiLayout &layout,
+                                  const bContext &C,
+                                  const StringRefNull asset_shelf_id,
+                                  const StringRef name,
+                                  const BIFIconID icon)
+{
+  AssetShelfType *shelf_type = ed::asset::shelf::type_find_from_idname(asset_shelf_id);
+  if (!shelf_type) {
+    RNA_warning("Asset shelf type not found: %s", asset_shelf_id.c_str());
+    return;
+  }
+
+  const ARegion *region = CTX_wm_region(&C);
+  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");
+  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);
+  }
+
+  if (ed::asset::shelf::type_poll_for_popup(C, shelf_type) == false) {
+    UI_but_flag_enable(but, UI_BUT_DISABLED);
+  }
+}
+
+}  // namespace blender::ui
diff --git a/source/blender/makesdna/DNA_screen_types.h b/source/blender/makesdna/DNA_screen_types.h
index f50a9a10625..6d610fc1614 100644
--- a/source/blender/makesdna/DNA_screen_types.h
+++ b/source/blender/makesdna/DNA_screen_types.h
@@ -833,6 +833,7 @@ typedef struct AssetShelf {
 
   AssetShelfSettings settings;
 
+  /** Only for the permanent asset shelf regions, not asset shelves in temporary popups. */
   short preferred_row_count;
   char _pad[6];
 } AssetShelf;
diff --git a/source/blender/makesrna/intern/rna_ui_api.cc b/source/blender/makesrna/intern/rna_ui_api.cc
index 86fffd5c54d..b0f260e0834 100644
--- a/source/blender/makesrna/intern/rna_ui_api.cc
+++ b/source/blender/makesrna/intern/rna_ui_api.cc
@@ -963,6 +963,20 @@ static int rna_ui_get_enum_icon(bContext *C,
   return icon;
 }
 
+void rna_uiTemplateAssetShelfPopover(uiLayout *layout,
+                                     bContext *C,
+                                     const char *asset_shelf_id,
+                                     const char *name,
+                                     BIFIconID icon,
+                                     int icon_value)
+{
+  if (icon_value && !icon) {
+    icon = icon_value;
+  }
+
+  blender::ui::template_asset_shelf_popover(*layout, *C, asset_shelf_id, name, icon);
+}
+
 #else
 
 static void api_ui_item_common_heading(FunctionRNA *func)
@@ -2287,6 +2301,25 @@ void RNA_api_ui_layout(StructRNA *srna)
   RNA_def_function_flag(func, FUNC_USE_CONTEXT);
   parm = RNA_def_pointer(func, "node", "Node", "Node", "Display inputs of this node");
   RNA_def_parameter_flags(parm, PROP_NEVER_NULL, PARM_REQUIRED | PARM_RNAPTR);
+
+  func = RNA_def_function(srna, "template_asset_shelf_popover", "rna_uiTemplateAssetShelfPopover");
+  RNA_def_function_ui_description(func, "Create a button to open an asset shelf in a popover");
+  RNA_def_function_flag(func, FUNC_USE_CONTEXT);
+  parm = RNA_def_string(func,
+                        "asset_shelf",
+                        nullptr,
+                        0,
+                        "",
+                        "Identifier of the asset shelf to display (`bl_idname`)");
+  RNA_def_parameter_flags(parm, PropertyFlag(0), PARM_REQUIRED);
+  parm = RNA_def_string(
+      func, "name", nullptr, 0, "", "Optional name to indicate the active asset");
+  RNA_def_property_clear_flag(parm, PROP_NEVER_NULL);
+  parm = RNA_def_property(func, "icon", PROP_ENUM, PROP_NONE);
+  RNA_def_property_enum_items(parm, rna_enum_icon_items);
+  RNA_def_property_ui_text(parm, "Icon", "Override automatic icon of the item");
+  parm = RNA_def_property(func, "icon_value", PROP_INT, PROP_UNSIGNED);
+  RNA_def_property_ui_text(parm, "Icon Value", "Override automatic icon of the item");
 }
 
 #endif