diff --git a/examples/reference/widgets/Tabulator.ipynb b/examples/reference/widgets/Tabulator.ipynb
index 206f252fbe..5d29793032 100644
--- a/examples/reference/widgets/Tabulator.ipynb
+++ b/examples/reference/widgets/Tabulator.ipynb
@@ -47,6 +47,7 @@
     "* **`groupby`** (`list`): Groups rows in the table by one or more columns.\n",
     "* **`header_align`** (`dict` or `str`): A mapping from column name to header alignment or a fixed header alignment, which should be one of `'left'`, `'center'`, `'right'`.\n",
     "* **`header_filters`** (`boolean`/`dict`): A boolean enabling filters in the column headers or a dictionary providing filter definitions for specific columns.\n",
+    "* **`header_tooltips`** (`dict`): Dictionary mapping from column name to a tooltip to show when hovering over the column header. \n",
     "* **`hidden_columns`** (`list`): List of columns to hide.\n",
     "* **`hierarchical`** (boolean, default=False): Whether to render multi-indexes as hierarchical index (note hierarchical must be enabled during instantiation and cannot be modified later)\n",
     "* **`initial_page_size`** (`int`, `default=20`): If pagination is enabled and `page_size` this determines the initial size of each page before rendering.\n",
diff --git a/panel/tests/ui/widgets/test_tabulator.py b/panel/tests/ui/widgets/test_tabulator.py
index 886975969a..4ba7cc8bde 100644
--- a/panel/tests/ui/widgets/test_tabulator.py
+++ b/panel/tests/ui/widgets/test_tabulator.py
@@ -3954,3 +3954,18 @@ def test_filtering_all(self, page):
             self.set_filtering(page, n)
             self.check_selected(page, list(range(10)), 0)
             expect(page.locator('.tabulator')).to_have_count(1)
+
+
+def test_tabulator_header_tooltips(page):
+    df = pd.DataFrame({"header": [True, False, True]})
+    widget = Tabulator(df, header_tooltips={"header": "Test"})
+
+    serve_component(page, widget)
+
+    header = page.locator('.tabulator-col-title', has_text="header")
+    expect(header).to_have_count(1)
+    header.hover()
+
+    page.wait_for_timeout(200)
+
+    expect(page.locator('.tabulator-tooltip')).to_have_text("Test")
diff --git a/panel/tests/widgets/test_tables.py b/panel/tests/widgets/test_tables.py
index 050acf1824..88af3e4905 100644
--- a/panel/tests/widgets/test_tables.py
+++ b/panel/tests/widgets/test_tables.py
@@ -2597,3 +2597,13 @@ def test_selection_cleared_remote_pagination_new_values(document, comm):
 
     table.value = df.copy()
     assert table.selection == []
+
+
+def test_save_user_columns_configuration(document, comm):
+    df = pd.DataFrame({"header": [True, False, True]})
+    configuration={"columns": [{"field": "header", "headerTooltip": True}]}
+    tabulator = Tabulator(df, configuration=configuration, show_index=False)
+
+    expected = [{'field': 'header', 'sorter': 'boolean', 'headerTooltip': True}]
+    model = tabulator.get_root(document, comm)
+    assert model.configuration["columns"] == expected
diff --git a/panel/widgets/tables.py b/panel/widgets/tables.py
index 7232f3736d..4641d8f97d 100644
--- a/panel/widgets/tables.py
+++ b/panel/widgets/tables.py
@@ -1129,6 +1129,10 @@ class Tabulator(BaseTable):
         Whether to enable filters in the header or dictionary
         configuring filters for each column.""")
 
+    header_tooltips = param.Dict(default={}, doc="""
+        Dictionary mapping from column name to a tooltip to show when
+        hovering over the column header.""")
+
     hidden_columns = param.List(default=[], nested_refs=True, doc="""
         List of columns to hide.""")
 
@@ -1220,7 +1224,7 @@ class Tabulator(BaseTable):
     _rename: ClassVar[Mapping[str, str | None]] = {
         'selection': None, 'row_content': None, 'row_height': None,
         'text_align': None, 'embed_content': None, 'header_align': None,
-        'header_filters': None, 'styles': 'cell_styles',
+        'header_filters': None, 'header_tooltips': None, 'styles': 'cell_styles',
         'title_formatters': None, 'sortable': None, 'initial_page_size': None
     }
 
@@ -1985,6 +1989,9 @@ def _config_columns(self, column_objs: list[TableColumn]) -> list[dict[str, Any]
                 col_dict['width'] = self.widths[field]
             col_dict.update(self._get_filter_spec(column))
 
+            if field in self.header_tooltips:
+                col_dict["headerTooltip"] = self.header_tooltips[field]
+
             if isinstance(index, tuple):
                 if columns:
                     children = columns
@@ -2029,7 +2036,11 @@ def _get_configuration(self, columns: list[dict[str, Any]]) -> dict[str, Any]:
         if self.groups and 'columns' in configuration:
             raise ValueError("Groups must be defined either explicitly "
                              "or via the configuration, not both.")
-        configuration['columns'] = self._config_columns(columns)
+        user_columns = {v["field"]: v for v in configuration.get('columns', {})}
+        configuration["columns"] = self._config_columns(columns)
+        for idx, col in enumerate(columns):
+            if (name := col.field) in user_columns:
+                configuration["columns"][idx] |= user_columns[name]
         configuration['dataTree'] = self.hierarchical
         if self.sizing_mode in ('stretch_height', 'stretch_both'):
             configuration['maxHeight'] = '100%'