diff --git a/docs/reference/hooks.md b/docs/reference/hooks.md
index 4f37b67ce7..819178082e 100644
--- a/docs/reference/hooks.md
+++ b/docs/reference/hooks.md
@@ -407,18 +407,29 @@ Return a QuerySet of `Permission` objects to be shown in the Groups administrati
 
 ### `register_user_listing_buttons`
 
-Add buttons to the user list. This example will add a simple button to the listing:
+Add buttons to the user list.
+
+This hook takes two parameters:
+-  `user`: The user object to generate the button for
+-  `request_user`: The currently logged-in user
+
+This example will add a simple button to the listing if the currently logged-in user is a superuser:
 
 ```python
 from wagtail.users.widgets import UserListingButton
 
 @hooks.register("register_user_listing_buttons")
-def user_listing_external_profile(context, user):
-    yield UserListingButton(
-        "Show profile",
-        f"/goes/to/a/url/{user.pk}",
-        priority=30,
-    )
+def user_listing_external_profile(user, request_user):
+    if request_user.is_superuser:
+        yield UserListingButton(
+            "Show profile",
+            f"/goes/to/a/url/{user.pk}",
+            priority=30,
+        )
+```
+
+```{versionchanged} 6.2
+The hook function was updated to accept a `request_user` argument instead of `context`.
 ```
 
 (filter_form_submissions_for_user)=
diff --git a/docs/releases/6.1.md b/docs/releases/6.1.md
index f817b78bf2..5e192b3bb9 100644
--- a/docs/releases/6.1.md
+++ b/docs/releases/6.1.md
@@ -108,8 +108,17 @@ As part of the Universal Listings project, the `SubmissionsListView` for listing
 - The `ordering` attribute has been renamed to `default_ordering`.
 - The template used to render the view has been significantly refactored to use the new universal listings UI.
 
+
+### `register_user_listing_buttons` hook signature changed
+
+The function signature for the [`register_user_listing_buttons`](register_user_listing_buttons) hook was updated to accept a `request_user` argument instead of `context`. If you use this hook, make sure to update your function signature to match the new one. The old signature with `context` will continue to work for now, but the context only contains the request object. Support for the old signature will be removed in a future release.
+
 ## Upgrade considerations - changes to undocumented internals
 
+### Deprecation of `user_listing_buttons` template tag
+
+The undocumented `user_listing_buttons` template tag has been deprecated and will be removed in a future release.
+
 ### Deprecation of `window.chooserUrls` within Draftail choosers
 
 The undocumented usage of the JavaScript `window.chooserUrls` within Draftail choosers will be removed in a future release.
diff --git a/wagtail/users/templatetags/wagtailusers_tags.py b/wagtail/users/templatetags/wagtailusers_tags.py
index 37603b37c6..bc4f6b922f 100644
--- a/wagtail/users/templatetags/wagtailusers_tags.py
+++ b/wagtail/users/templatetags/wagtailusers_tags.py
@@ -1,5 +1,5 @@
-import itertools
 from collections import defaultdict
+from warnings import warn
 
 from django import template
 from django.contrib.auth import get_permission_codename
@@ -9,7 +9,9 @@ from django.utils.text import camel_case_to_spaces
 
 from wagtail import hooks
 from wagtail.admin.models import Admin
+from wagtail.coreutils import accepts_kwarg
 from wagtail.users.permission_order import CONTENT_TYPE_ORDER
+from wagtail.utils.deprecation import RemovedInWagtail70Warning
 
 register = template.Library()
 
@@ -185,8 +187,24 @@ def format_permissions(permission_bound_field):
 
 @register.inclusion_tag("wagtailadmin/shared/buttons.html", takes_context=True)
 def user_listing_buttons(context, user):
-    button_hooks = hooks.get_hooks("register_user_listing_buttons")
-    buttons = sorted(
-        itertools.chain.from_iterable(hook(context, user) for hook in button_hooks)
+    warn(
+        "`user_listing_buttons` template tag is deprecated.",
+        category=RemovedInWagtail70Warning,
     )
-    return {"user": user, "buttons": buttons}
+
+    buttons = []
+
+    for hook in hooks.get_hooks("register_user_listing_buttons"):
+        if accepts_kwarg(hook, "request_user"):
+            buttons.extend(hook(user=user, request_user=context.get("request").user))
+        else:
+            # old-style hook that accepts a context argument instead of request_user
+            buttons.extend(hook(context, user))
+            warn(
+                "`register_user_listing_buttons` hook functions should accept a "
+                "`request_user` argument instead of `context` - "
+                f"{hook.__module__}.{hook.__name__} needs to be updated",
+                category=RemovedInWagtail70Warning,
+            )
+
+    return {"user": user, "buttons": sorted(buttons)}
diff --git a/wagtail/users/tests/test_admin_views.py b/wagtail/users/tests/test_admin_views.py
index 20654eae7e..0087ba4b4d 100644
--- a/wagtail/users/tests/test_admin_views.py
+++ b/wagtail/users/tests/test_admin_views.py
@@ -10,6 +10,7 @@ from django.core.exceptions import ImproperlyConfigured
 from django.core.files.uploadedfile import SimpleUploadedFile
 from django.db.models import Q
 from django.http import HttpRequest, HttpResponse
+from django.template import RequestContext, Template
 from django.test import TestCase, override_settings
 from django.urls import reverse
 from django.utils.text import capfirst
@@ -18,7 +19,9 @@ from wagtail import hooks
 from wagtail.admin.admin_url_finder import AdminURLFinder
 from wagtail.admin.models import Admin
 from wagtail.admin.staticfiles import versioned_static
+from wagtail.admin.widgets.button import ButtonWithDropdown
 from wagtail.compat import AUTH_USER_APP_LABEL, AUTH_USER_MODEL_NAME
+from wagtail.coreutils import get_dummy_request
 from wagtail.log_actions import log
 from wagtail.models import (
     Collection,
@@ -34,6 +37,7 @@ from wagtail.users.permission_order import register as register_permission_order
 from wagtail.users.views.groups import GroupViewSet
 from wagtail.users.views.users import get_user_creation_form, get_user_edit_form
 from wagtail.users.wagtail_hooks import get_group_viewset_cls
+from wagtail.users.widgets import UserListingButton
 from wagtail.utils.deprecation import RemovedInWagtail70Warning
 
 delete_user_perm_codename = f"delete_{AUTH_USER_MODEL_NAME.lower()}"
@@ -197,7 +201,7 @@ class TestUserIndexView(AdminTemplateTestUtils, WagtailTestUtils, TestCase):
             first_name="First Name",
             last_name="Last Name",
         )
-        self.login()
+        self.user = self.login()
 
     def get(self, params={}):
         return self.client.get(reverse("wagtailusers_users:index"), params)
@@ -273,6 +277,60 @@ class TestUserIndexView(AdminTemplateTestUtils, WagtailTestUtils, TestCase):
         with self.assertNumQueries(num_queries):
             self.get()
 
+    def test_buttons_hook(self):
+        def hook(user, request_user):
+            self.assertEqual(request_user, self.user)
+            yield UserListingButton(
+                "Show profile",
+                f"/goes/to/a/url/{user.pk}",
+                priority=30,
+            )
+            yield ButtonWithDropdown(
+                label="Moar pls!",
+                buttons=[UserListingButton("Alrighty", "/cheers", priority=10)],
+            )
+
+        with self.register_hook("register_user_listing_buttons", hook):
+            response = self.get()
+
+        self.assertEqual(response.status_code, 200)
+        self.assertTemplateUsed(response, "wagtailadmin/shared/buttons.html")
+
+        soup = self.get_soup(response.content)
+        row = soup.select_one(f"tbody tr:has([data-object-id='{self.test_user.pk}'])")
+        self.assertIsNotNone(row)
+
+        profile_url = f"/goes/to/a/url/{self.test_user.pk}"
+        actions = row.select_one("td ul.actions")
+        top_level_custom_button = actions.select_one(f"li > a[href='{profile_url}']")
+        self.assertIsNone(top_level_custom_button)
+        custom_button = actions.select_one(
+            f"li [data-controller='w-dropdown'] a[href='{profile_url}']"
+        )
+        self.assertIsNotNone(custom_button)
+        self.assertEqual(
+            custom_button.text.strip(),
+            "Show profile",
+        )
+
+        nested_dropdown = actions.select_one(
+            "li [data-controller='w-dropdown'] [data-controller='w-dropdown']"
+        )
+        self.assertIsNone(nested_dropdown)
+        dropdown_buttons = actions.select("li > [data-controller='w-dropdown']")
+        # Default "More" button and the custom "Moar pls!" button
+        self.assertEqual(len(dropdown_buttons), 2)
+        custom_dropdown = None
+        for button in dropdown_buttons:
+            if "Moar pls!" in button.text.strip():
+                custom_dropdown = button
+        self.assertIsNotNone(custom_dropdown)
+        self.assertEqual(custom_dropdown.select_one("button").text.strip(), "Moar pls!")
+        # Should contain the custom button inside the custom dropdown
+        custom_button = custom_dropdown.find("a", attrs={"href": "/cheers"})
+        self.assertIsNotNone(custom_button)
+        self.assertEqual(custom_button.text.strip(), "Alrighty")
+
 
 class TestUserIndexResultsView(AdminTemplateTestUtils, WagtailTestUtils, TestCase):
     def setUp(self):
@@ -2637,3 +2695,100 @@ class TestAuthorisationDeleteView(WagtailTestUtils, TestCase):
         self.assertRedirects(response, reverse("wagtailusers_users:index"))
         user = get_user_model().objects.filter(email="test_user@email.com")
         self.assertFalse(user.exists())
+
+
+class TestTemplateTags(WagtailTestUtils, TestCase):
+    @classmethod
+    def setUpTestData(cls):
+        cls.user = cls.create_superuser("admin")
+        cls.request = get_dummy_request()
+        cls.request.user = cls.user
+        cls.test_user = cls.create_user(
+            username="testuser",
+            email="testuser@email.com",
+            password="password",
+        )
+
+    def test_user_listing_buttons(self):
+        template = """
+            {% load wagtailusers_tags %}
+            {% for user in users %}
+                <ul class="actions">
+                    {% user_listing_buttons user %}
+                </ul>
+            {% endfor %}
+        """
+
+        def hook(user, request_user):
+            self.assertEqual(user, self.test_user)
+            self.assertEqual(request_user, self.user)
+            yield UserListingButton(
+                "Show profile",
+                f"/goes/to/a/url/{user.pk}",
+                priority=30,
+            )
+
+        with self.register_hook("register_user_listing_buttons", hook):
+            with self.assertWarnsMessage(
+                RemovedInWagtail70Warning,
+                "`user_listing_buttons` template tag is deprecated.",
+            ):
+                html = Template(template).render(
+                    RequestContext(self.request, {"users": [self.test_user]})
+                )
+
+        soup = self.get_soup(html)
+
+        profile_url = f"/goes/to/a/url/{self.test_user.pk}"
+        top_level_custom_button = soup.select_one(f"li > a[href='{profile_url}']")
+        self.assertIsNotNone(top_level_custom_button)
+        self.assertEqual(
+            top_level_custom_button.text.strip(),
+            "Show profile",
+        )
+
+    def test_user_listing_buttons_with_deprecated_hook(self):
+        template = """
+            {% load wagtailusers_tags %}
+            {% for user in users %}
+                <ul class="actions">
+                    {% user_listing_buttons user %}
+                </ul>
+            {% endfor %}
+        """
+
+        def deprecated_hook(context, user):
+            self.assertEqual(user, self.test_user)
+            self.assertEqual(context.request.user, self.user)
+            yield UserListingButton(
+                "Show profile",
+                f"/goes/to/a/url/{user.pk}",
+                priority=30,
+            )
+
+        with self.register_hook("register_user_listing_buttons", deprecated_hook):
+            with self.assertWarns(RemovedInWagtail70Warning) as warning_manager:
+                html = Template(template).render(
+                    RequestContext(self.request, {"users": [self.test_user]})
+                )
+
+        self.assertEqual(
+            [str(w.message) for w in warning_manager.warnings],
+            [
+                # Deprecation of the template tag
+                "`user_listing_buttons` template tag is deprecated.",
+                # Deprecation of the hook signature
+                "`register_user_listing_buttons` hook functions should accept a "
+                "`request_user` argument instead of `context` - "
+                "wagtail.users.tests.test_admin_views.deprecated_hook needs to be updated",
+            ],
+        )
+
+        soup = self.get_soup(html)
+        profile_url = f"/goes/to/a/url/{self.test_user.pk}"
+        top_level_custom_button = soup.select_one(f"li > a[href='{profile_url}']")
+        self.assertIsNotNone(top_level_custom_button)
+        self.assertEqual(
+            top_level_custom_button.text.strip(),
+            "Show profile",
+        )
diff --git a/wagtail/users/views/users.py b/wagtail/users/views/users.py
index b7fade35aa..f8010b62db 100644
--- a/wagtail/users/views/users.py
+++ b/wagtail/users/views/users.py
@@ -1,3 +1,5 @@
+from warnings import warn
+
 from django.conf import settings
 from django.contrib.auth import get_user_model, update_session_auth_hash
 from django.contrib.auth.models import Group
@@ -26,9 +28,11 @@ from wagtail.admin.widgets.button import (
     ButtonWithDropdown,
 )
 from wagtail.compat import AUTH_USER_APP_LABEL, AUTH_USER_MODEL_NAME
+from wagtail.coreutils import accepts_kwarg
 from wagtail.permission_policies import ModelPermissionPolicy
 from wagtail.users.forms import UserCreationForm, UserEditForm
 from wagtail.users.utils import user_can_delete_user
+from wagtail.utils.deprecation import RemovedInWagtail70Warning
 from wagtail.utils.loading import get_custom_form
 
 User = get_user_model()
@@ -172,7 +176,17 @@ class Index(IndexView):
         list_buttons = []
 
         for hook in hooks.get_hooks("register_user_listing_buttons"):
-            hook_buttons = hook(RequestContext(self.request), instance)
+            if accepts_kwarg(hook, "request_user"):
+                hook_buttons = hook(user=instance, request_user=self.request.user)
+            else:
+                # old-style hook that accepts a context argument instead of request_user
+                hook_buttons = hook(RequestContext(self.request), instance)
+                warn(
+                    "`register_user_listing_buttons` hook functions should accept a `request_user` argument instead of `context` -"
+                    f" {hook.__module__}.{hook.__name__} needs to be updated",
+                    category=RemovedInWagtail70Warning,
+                )
+
             for button in hook_buttons:
                 if isinstance(button, BaseDropdownMenuButton):
                     # If the button is a dropdown menu, add it to the top-level