diff --git a/datasette/app.py b/datasette/app.py
index 57f893fe..9c9b7de4 100644
--- a/datasette/app.py
+++ b/datasette/app.py
@@ -12,7 +12,6 @@ import dataclasses
 import datetime
 import functools
 import glob
-import hashlib
 import httpx
 import importlib.metadata
 import inspect
@@ -123,6 +122,7 @@ from .utils import (
     parse_metadata,
     resolve_env_secrets,
     resolve_routes,
+    sha256_file,
     tilde_decode,
     tilde_encode,
     to_css_class,
@@ -314,7 +314,7 @@ async def favicon(request, send):
         send,
         str(FAVICON_PATH),
         content_type="image/png",
-        headers={"Cache-Control": "max-age=3600, immutable, public"},
+        headers={"Cache-Control": "max-age=3600, public"},
     )
 
 
@@ -348,6 +348,16 @@ def _legacy_template_csrftoken(context):
     return ""
 
 
+def _resolve_static_asset_path(root_path, path):
+    root = Path(root_path).resolve()
+    full_path = (root / path).resolve()
+    try:
+        full_path.relative_to(root)
+    except ValueError:
+        raise ValueError("Static asset path cannot escape static root") from None
+    return full_path
+
+
 # Documentation for the variables Datasette.render_template() adds to the
 # context for every page. This is part of the documented template contract:
 # keys added in render_template() must be documented here - the contract
@@ -361,9 +371,6 @@ TEMPLATE_BASE_CONTEXT = {
     "menu_links": "Async function returning links for the Datasette application menu, including links added by plugins. Each item is a link dictionary with ``href`` and ``label`` keys. See :ref:`plugin_hook_menu_links`; for page action menus that can also include JavaScript-backed buttons, see :ref:`plugin_actions`.",
     "display_actor": "Function that accepts an actor dictionary and returns the display string used in the navigation menu.",
     "show_logout": "True if the logout link should be shown in the navigation menu",
-    "app_css_hash": "Hash of Datasette's app.css contents, used for cache busting",
-    "edit_tools_js_hash": "Hash of Datasette's edit-tools.js contents, used for cache busting",
-    "table_js_hash": "Hash of Datasette's table.js contents, used for cache busting",
     "zip": "Python's ``zip()`` builtin, made available to template logic",
     "body_scripts": 'List of JavaScript snippets contributed by plugins using :ref:`plugin_hook_extra_body_script`. Each item is a dictionary with ``script`` containing JavaScript source and ``module`` indicating whether Datasette will wrap it in ``<script type="module">``; otherwise Datasette wraps it in a regular ``<script>`` block.',
     "format_bytes": "Function that accepts a byte count integer and returns a human-readable string such as ``1.2 MB``.",
@@ -467,6 +474,7 @@ class Datasette:
         self._internal_database.name = INTERNAL_DB_NAME
 
         self.cache_headers = cache_headers
+        self._static_asset_hashes = {}
         self.cors = cors
         config_files = []
         metadata_files = []
@@ -608,6 +616,7 @@ class Datasette:
         environment.filters["escape_css_string"] = escape_css_string
         environment.filters["quote_plus"] = urllib.parse.quote_plus
         environment.globals["csrftoken"] = _legacy_template_csrftoken
+        environment.globals["static"] = self.static
         self._jinja_env = environment
         environment.filters["escape_sqlite"] = escape_sqlite
         environment.filters["to_css_class"] = to_css_class
@@ -1481,24 +1490,55 @@ class Datasette:
 
         return db_plugin_config
 
-    def static_hash(self, filename):
-        if not hasattr(self, "_static_hashes"):
-            self._static_hashes = {}
-        path = os.path.join(str(app_root), "datasette/static", filename)
-        signature = (os.path.getmtime(path), os.path.getsize(path))
-        cached = self._static_hashes.get(filename)
-        if cached and cached["signature"] == signature:
-            return cached["hash"]
-        with open(path) as fp:
-            static_hash = hashlib.sha1(fp.read().encode("utf8")).hexdigest()[:6]
-        self._static_hashes[filename] = {
-            "signature": signature,
-            "hash": static_hash,
-        }
-        return static_hash
+    def _static_asset_path(self, path):
+        return _resolve_static_asset_path(app_root / "datasette" / "static", path)
 
-    def app_css_hash(self):
-        return self.static_hash("app.css")
+    def _static_plugin_asset_path(self, plugin_name, path):
+        for plugin in get_plugins():
+            if not plugin["static_path"]:
+                continue
+            possible_names = {plugin["name"], plugin["name"].replace("-", "_")}
+            if plugin_name in possible_names:
+                return _resolve_static_asset_path(plugin["static_path"], path)
+        raise FileNotFoundError(
+            "No static assets found for plugin {}".format(plugin_name)
+        )
+
+    def _static_mounted_asset(self, mount_name, path):
+        mount_name = mount_name.strip("/")
+        for mount, dirname in self.static_mounts:
+            if mount.strip("/") == mount_name:
+                return (
+                    _resolve_static_asset_path(dirname, path),
+                    self.urls.path("/{}/{}".format(mount_name, path.lstrip("/"))),
+                )
+        raise FileNotFoundError("No static mount found for {}".format(mount_name))
+
+    def _static_asset_hash(self, filepath):
+        filepath = Path(filepath)
+        if self.cache_headers:
+            cached = self._static_asset_hashes.get(filepath)
+            if cached:
+                return cached
+        digest = sha256_file(filepath)[:12]
+        if self.cache_headers:
+            self._static_asset_hashes[filepath] = digest
+        return digest
+
+    def static(self, path, plugin=None, mount=None):
+        if plugin and mount:
+            raise ValueError("Use either plugin= or mount=, not both")
+        if plugin:
+            filepath = self._static_plugin_asset_path(plugin, path)
+            url = self.urls.static_plugins(plugin, path)
+        elif mount:
+            filepath, url = self._static_mounted_asset(mount, path)
+        else:
+            filepath = self._static_asset_path(path)
+            url = self.urls.static(path)
+        hash_value = self._static_asset_hash(filepath)
+        separator = "&" if "?" in url else "?"
+        return url + separator + urllib.parse.urlencode({"_hash": hash_value})
 
     def _prepare_connection(self, conn, database):
         conn.row_factory = sqlite3.Row
@@ -2379,9 +2419,6 @@ class Datasette:
                 "show_logout": request is not None
                 and "ds_actor" in request.cookies
                 and request.actor,
-                "app_css_hash": self.app_css_hash(),
-                "edit_tools_js_hash": self.static_hash("edit-tools.js"),
-                "table_js_hash": self.static_hash("table.js"),
                 "zip": zip,
                 "body_scripts": body_scripts,
                 "format_bytes": format_bytes,
@@ -2480,7 +2517,6 @@ class Datasette:
         add_route(IndexView.as_view(self), r"/(\.(?P<format>jsono?))?$")
         add_route(IndexView.as_view(self), r"/-/(\.(?P<format>jsono?))?$")
         add_route(permanent_redirect("/-/"), r"/-$")
-        # TODO: /favicon.ico and /-/static/ deserve far-future cache expires
         add_route(favicon, "/favicon.ico")
 
         add_route(
diff --git a/datasette/handle_exception.py b/datasette/handle_exception.py
index 96398a4c..2b311644 100644
--- a/datasette/handle_exception.py
+++ b/datasette/handle_exception.py
@@ -66,7 +66,6 @@ def handle_exception(datasette, request, exception):
                     dict(
                         info,
                         urls=datasette.urls,
-                        app_css_hash=datasette.app_css_hash(),
                         menu_links=lambda: [],
                     )
                 ),
diff --git a/datasette/templates/_codemirror.html b/datasette/templates/_codemirror.html
index c4629aeb..75c16168 100644
--- a/datasette/templates/_codemirror.html
+++ b/datasette/templates/_codemirror.html
@@ -1,5 +1,5 @@
-<script src="{{ base_url }}-/static/sql-formatter-2.3.3.min.js" defer></script>
-<script src="{{ base_url }}-/static/cm-editor-6.0.1.bundle.js"></script>
+<script src="{{ static('sql-formatter-2.3.3.min.js') }}" defer></script>
+<script src="{{ static('cm-editor-6.0.1.bundle.js') }}"></script>
 <style>
   .cm-editor {
     resize: both;
diff --git a/datasette/templates/api_explorer.html b/datasette/templates/api_explorer.html
index 58e2a88c..4927cb8d 100644
--- a/datasette/templates/api_explorer.html
+++ b/datasette/templates/api_explorer.html
@@ -3,7 +3,7 @@
 {% block title %}API Explorer{% endblock %}
 
 {% block extra_head %}
-<script src="{{ base_url }}-/static/json-format-highlight-1.0.1.js"></script>
+<script src="{{ static('json-format-highlight-1.0.1.js') }}"></script>
 {% endblock %}
 
 {% block content %}
diff --git a/datasette/templates/base.html b/datasette/templates/base.html
index 82ab48dd..18288439 100644
--- a/datasette/templates/base.html
+++ b/datasette/templates/base.html
@@ -2,13 +2,13 @@
 <html lang="en">
 <head>
     <title>{% block title %}{% endblock %}</title>
-    <link rel="stylesheet" href="{{ urls.static('app.css') }}?{{ app_css_hash }}">
+    <link rel="stylesheet" href="{{ static('app.css') }}">
     <meta name="viewport" content="width=device-width, initial-scale=1, shrink-to-fit=no">
 {% for url in extra_css_urls %}
     <link rel="stylesheet" href="{{ url.url }}"{% if url.get("sri") %} integrity="{{ url.sri }}" crossorigin="anonymous"{% endif %}>
 {% endfor %}
 <script>window.datasetteVersion = '{{ datasette_version }}';</script>
-<script src="{{ urls.static('datasette-manager.js') }}" defer></script>
+<script src="{{ static('datasette-manager.js') }}" defer></script>
 {% for url in extra_js_urls %}
     <script {% if url.module %}type="module" {% endif %}src="{{ url.url }}"{% if url.get("sri") %} integrity="{{ url.sri }}" crossorigin="anonymous"{% endif %}></script>
 {% endfor %}
@@ -70,7 +70,7 @@
 {% endfor %}
 
 {% if select_templates %}<!-- Templates considered: {{ select_templates|join(", ") }} -->{% endif %}
-<script src="{{ urls.static('navigation-search.js') }}" defer></script>
+<script src="{{ static('navigation-search.js') }}" defer></script>
 <navigation-search url="{{ urls.path("/-/jump") }}"></navigation-search>
 </body>
 </html>
diff --git a/datasette/templates/database.html b/datasette/templates/database.html
index c09582f7..a9fad8dd 100644
--- a/datasette/templates/database.html
+++ b/datasette/templates/database.html
@@ -8,7 +8,7 @@
 {% include "_sql_parameter_styles.html" %}
 {% if database_page_data.createTable %}
 <script>window._datasetteDatabaseData = {{ database_page_data|tojson }};</script>
-<script src="{{ urls.static('edit-tools.js') }}?hash={{ edit_tools_js_hash }}" defer></script>
+<script src="{{ static('edit-tools.js') }}" defer></script>
 {% endif %}
 {% endblock %}
 
diff --git a/datasette/templates/debug_allowed.html b/datasette/templates/debug_allowed.html
index add3154a..4f8106b8 100644
--- a/datasette/templates/debug_allowed.html
+++ b/datasette/templates/debug_allowed.html
@@ -3,7 +3,7 @@
 {% block title %}Allowed Resources{% endblock %}
 
 {% block extra_head %}
-<script src="{{ base_url }}-/static/json-format-highlight-1.0.1.js"></script>
+<script src="{{ static('json-format-highlight-1.0.1.js') }}"></script>
 {% include "_permission_ui_styles.html" %}
 {% include "_debug_common_functions.html" %}
 {% endblock %}
diff --git a/datasette/templates/debug_autocomplete.html b/datasette/templates/debug_autocomplete.html
index 84dbc14f..380639a3 100644
--- a/datasette/templates/debug_autocomplete.html
+++ b/datasette/templates/debug_autocomplete.html
@@ -4,7 +4,7 @@
 
 {% block extra_head %}
 {{ super() }}
-<script src="{{ urls.static('autocomplete.js') }}" defer></script>
+<script src="{{ static('autocomplete.js') }}" defer></script>
 {% endblock %}
 
 {% block content %}
diff --git a/datasette/templates/debug_check.html b/datasette/templates/debug_check.html
index c2e7997f..3b229a25 100644
--- a/datasette/templates/debug_check.html
+++ b/datasette/templates/debug_check.html
@@ -3,7 +3,7 @@
 {% block title %}Permission Check{% endblock %}
 
 {% block extra_head %}
-<script src="{{ base_url }}-/static/json-format-highlight-1.0.1.js"></script>
+<script src="{{ static('json-format-highlight-1.0.1.js') }}"></script>
 {% include "_permission_ui_styles.html" %}
 {% include "_debug_common_functions.html" %}
 <style>
diff --git a/datasette/templates/debug_rules.html b/datasette/templates/debug_rules.html
index 9a290803..aafa755d 100644
--- a/datasette/templates/debug_rules.html
+++ b/datasette/templates/debug_rules.html
@@ -3,7 +3,7 @@
 {% block title %}Permission Rules{% endblock %}
 
 {% block extra_head %}
-<script src="{{ base_url }}-/static/json-format-highlight-1.0.1.js"></script>
+<script src="{{ static('json-format-highlight-1.0.1.js') }}"></script>
 {% include "_permission_ui_styles.html" %}
 {% include "_debug_common_functions.html" %}
 {% endblock %}
diff --git a/datasette/templates/patterns.html b/datasette/templates/patterns.html
index bff44341..075c0117 100644
--- a/datasette/templates/patterns.html
+++ b/datasette/templates/patterns.html
@@ -2,7 +2,7 @@
 <html lang="en">
 <head>
     <title>Datasette: Pattern Portfolio</title>
-    <link rel="stylesheet" href="{{ base_url }}-/static/app.css?{{ app_css_hash }}">
+    <link rel="stylesheet" href="{{ static('app.css') }}">
     <meta name="viewport" content="width=device-width, initial-scale=1, shrink-to-fit=no">
     <meta name="robots" content="noindex">
     <style></style>
diff --git a/datasette/templates/row.html b/datasette/templates/row.html
index 5e483d34..aa1f0ecd 100644
--- a/datasette/templates/row.html
+++ b/datasette/templates/row.html
@@ -7,9 +7,9 @@
 {% if row_mutation_ui %}
 <script>window._datasetteTableData = {{ table_page_data|tojson }};</script>
 {% if table_page_data.foreignKeys %}
-<script src="{{ urls.static('autocomplete.js') }}" defer></script>
+<script src="{{ static('autocomplete.js') }}" defer></script>
 {% endif %}
-<script src="{{ urls.static('edit-tools.js') }}?hash={{ edit_tools_js_hash }}" defer></script>
+<script src="{{ static('edit-tools.js') }}" defer></script>
 {% endif %}
 <style>
 @media only screen and (max-width: 576px) {
diff --git a/datasette/templates/table.html b/datasette/templates/table.html
index b7b776ab..c2131360 100644
--- a/datasette/templates/table.html
+++ b/datasette/templates/table.html
@@ -5,13 +5,13 @@
 {% block extra_head %}
 {{- super() -}}
 <script>window._datasetteTableData = {{ table_page_data|tojson }};</script>
-<script src="{{ urls.static('column-chooser.js') }}" defer></script>
+<script src="{{ static('column-chooser.js') }}" defer></script>
 {% if table_page_data.foreignKeys %}
-<script src="{{ urls.static('autocomplete.js') }}" defer></script>
+<script src="{{ static('autocomplete.js') }}" defer></script>
 {% endif %}
-<script src="{{ urls.static('edit-tools.js') }}?hash={{ edit_tools_js_hash }}" defer></script>
-<script src="{{ urls.static('table.js') }}?hash={{ table_js_hash }}" defer></script>
-<script src="{{ urls.static('mobile-column-actions.js') }}" defer></script>
+<script src="{{ static('edit-tools.js') }}" defer></script>
+<script src="{{ static('table.js') }}" defer></script>
+<script src="{{ static('mobile-column-actions.js') }}" defer></script>
 <script>DATASETTE_ALLOW_FACET = {{ datasette_allow_facet }};</script>
 <style>
 @media only screen and (max-width: 576px) {
diff --git a/datasette/utils/__init__.py b/datasette/utils/__init__.py
index 55e539b9..9174dca7 100644
--- a/datasette/utils/__init__.py
+++ b/datasette/utils/__init__.py
@@ -1548,6 +1548,17 @@ def md5_not_usedforsecurity(s):
 _etag_cache = {}
 
 
+def sha256_file(filepath, chunk_size=4096):
+    hasher = hashlib.sha256()
+    with open(filepath, "rb") as fp:
+        while True:
+            chunk = fp.read(chunk_size)
+            if not chunk:
+                break
+            hasher.update(chunk)
+    return hasher.hexdigest()
+
+
 async def calculate_etag(filepath, chunk_size=4096):
     if filepath in _etag_cache:
         return _etag_cache[filepath]
diff --git a/datasette/utils/asgi.py b/datasette/utils/asgi.py
index 93084365..e1631b10 100644
--- a/datasette/utils/asgi.py
+++ b/datasette/utils/asgi.py
@@ -1,6 +1,6 @@
 import json
 from typing import Optional
-from datasette.utils import MultiParams, calculate_etag
+from datasette.utils import MultiParams, calculate_etag, sha256_file
 from datasette.utils.multipart import (
     parse_form_data,
     MultipartParseError,
@@ -397,6 +397,9 @@ async def asgi_send_file(
             )
 
 
+HASHED_STATIC_CACHE_CONTROL = "max-age=31536000, immutable, public"
+
+
 def asgi_static(root_path, chunk_size=4096, headers=None, content_type=None):
     root_path = Path(root_path)
     static_headers = {}
@@ -423,11 +426,17 @@ def asgi_static(root_path, chunk_size=4096, headers=None, content_type=None):
             return
         try:
             # Calculate ETag for filepath
+            hash_value = request.args.get("_hash")
+            if (
+                hash_value
+                and hash_value == sha256_file(full_path, chunk_size=chunk_size)[:12]
+            ):
+                headers["Cache-Control"] = HASHED_STATIC_CACHE_CONTROL
             etag = await calculate_etag(full_path, chunk_size=chunk_size)
             headers["ETag"] = etag
             if_none_match = request.headers.get("if-none-match")
             if if_none_match and if_none_match == etag:
-                return await asgi_send(send, "", 304)
+                return await asgi_send(send, "", 304, headers=headers)
             await asgi_send_file(
                 send, full_path, chunk_size=chunk_size, headers=headers
             )
diff --git a/docs/changelog.rst b/docs/changelog.rst
index 01ef7f18..3ad8e0da 100644
--- a/docs/changelog.rst
+++ b/docs/changelog.rst
@@ -15,7 +15,8 @@ Unreleased
 - Create and alter table dialogs share their column-editing controls, including literal and expression defaults, custom column types, foreign keys and column ordering.
 - The "Write to this database" page now includes a Create table starter template, alongside the existing Insert, Update and Delete templates. (:pr:`2794`)
 - New :ref:`template_context` documentation listing the variables available to custom templates for Datasette's core pages. Variables documented there are treated as a stable API for custom templates until Datasette 2.0. The documentation is generated from dataclass definitions next to the view code, with tests that compare the documented fields against the actual contexts rendered by the database, table, query and row pages. (:issue:`1510`, :issue:`2127`, :issue:`1477`, :pr:`2803`)
-- Database and table pages now use the ``count_truncated`` template context value to display capped row counts as ``>N rows`.
+- New ``static()`` template function and ``datasette.static()`` method for generating cache-busting static asset URLs based on the file contents. Static assets served with a matching ``?_hash=`` parameter now receive far-future immutable cache headers. This works for Datasette's bundled static assets, plugin static assets and directories mounted using ``--static``. See :ref:`customization_static_files`.
+- Database and table pages now use the ``count_truncated`` template context value to display capped row counts as ``>N rows``.
 - Significant visual improvements to the table filter form UI, plus working add/remove filter buttons. (:issue:`2798`)
 - Improved edit row icon on table pages. (:issue:`2796`)
 
diff --git a/docs/contributing.rst b/docs/contributing.rst
index 142c2f41..692f94c8 100644
--- a/docs/contributing.rst
+++ b/docs/contributing.rst
@@ -157,6 +157,9 @@ If you want to change Datasette's Python code you can use the ``--reload`` optio
 
     uv run datasette --reload fixtures.db
 
+This also enables development mode for static asset cache busting, described in
+:ref:`customization_static_files`.
+
 You can also use the ``fixtures.py`` script to recreate the testing version of ``metadata.json`` used by the unit tests. To do that::
 
     uv run python tests/fixtures.py fixtures.db fixtures-metadata.json
diff --git a/docs/custom_templates.rst b/docs/custom_templates.rst
index f28f1189..bfbd1725 100644
--- a/docs/custom_templates.rst
+++ b/docs/custom_templates.rst
@@ -151,6 +151,45 @@ You can reference those files from ``datasette.yaml`` like this, see :ref:`custo
         }
 .. [[[end]]]
 
+If you reference those files from a custom template, use the ``static()``
+template function to create a cache-busting URL based on the file contents.
+Pass the mount point as the ``mount=`` argument, and pass a path relative to
+that mounted directory:
+
+.. code-block:: html+jinja
+
+    <link rel="stylesheet" href="{{ static('styles.css', mount='assets') }}">
+    <script src="{{ static('app.js', mount='assets') }}" defer></script>
+
+The returned URL will include a ``?_hash=`` parameter and will take the
+``base_url`` setting into account. When that hash matches the current file
+contents, Datasette will serve the static asset with a far-future immutable
+``Cache-Control`` header. You can also use ``urls.path()`` if you want to link
+to the mounted file without adding a content hash:
+
+.. code-block:: html+jinja
+
+    <link rel="stylesheet" href="{{ urls.path('/assets/styles.css') }}">
+
+When Datasette is run using ``--reload``, the file contents are hashed every time
+the template is rendered, so edits to static files will update their URLs
+without restarting Datasette. Without ``--reload``, the hash is cached for the
+lifetime of the Datasette process.
+
+You can use the same function for Datasette's bundled static assets, omitting
+``mount=``:
+
+.. code-block:: html+jinja
+
+    <link rel="stylesheet" href="{{ static('app.css') }}">
+
+For plugin static assets, pass the plugin name using ``plugin=`` and a path
+relative to the plugin's ``static/`` directory:
+
+.. code-block:: html+jinja
+
+    <script src="{{ static('plugin.js', plugin='datasette_plugin_name') }}" defer></script>
+
 Publishing static assets
 ~~~~~~~~~~~~~~~~~~~~~~~~
 
diff --git a/docs/internals.rst b/docs/internals.rst
index 06027f42..c826de1a 100644
--- a/docs/internals.rst
+++ b/docs/internals.rst
@@ -451,6 +451,52 @@ await .render_template(template, context=None, request=None)
 
 Renders a `Jinja template <https://jinja.palletsprojects.com/en/2.11.x/>`__ using Datasette's preconfigured instance of Jinja and returns the resulting string. The template will have access to Datasette's default template functions and any functions that have been made available by other plugins.
 
+.. _datasette_static:
+
+.static(path, plugin=None, mount=None)
+--------------------------------------
+
+``path`` - string
+    The path to the static asset, relative to the selected static directory.
+
+``plugin`` - string, optional
+    The plugin name, for linking to an asset in that plugin's ``static/``
+    directory.
+
+``mount`` - string, optional
+    The ``--static`` mount name, for linking to an asset in a directory mounted
+    using ``datasette --static mount_name:directory``.
+
+Returns a URL for a static asset with a ``?_hash=`` parameter based on the file
+contents. That URL takes the ``base_url`` setting into account.
+
+When the ``?_hash=`` parameter matches the current file contents, Datasette will
+serve the asset with ``Cache-Control: max-age=31536000, immutable, public``.
+
+Call this with just ``path`` for one of Datasette's bundled static assets:
+
+.. code-block:: python
+
+    datasette.static("app.css")
+
+Use ``plugin=`` for plugin static assets:
+
+.. code-block:: python
+
+    datasette.static(
+        "plugin.js", plugin="datasette_plugin_name"
+    )
+
+Use ``mount=`` for static directories mounted using the ``--static`` option:
+
+.. code-block:: python
+
+    datasette.static("styles.css", mount="assets")
+
+``plugin`` and ``mount`` are mutually exclusive. The same feature is available
+to Jinja templates as the ``static()`` template function, described in
+:ref:`customization_static_files`.
+
 .. _datasette_actors_from_ids:
 
 await .actors_from_ids(actor_ids)
diff --git a/docs/plugin_hooks.rst b/docs/plugin_hooks.rst
index 66419ec4..81ef4acd 100644
--- a/docs/plugin_hooks.rst
+++ b/docs/plugin_hooks.rst
@@ -1968,9 +1968,8 @@ Here is a minimal plugin example that adds a button to a table page and loads Ja
     @hookimpl
     def extra_js_urls(datasette):
         return [
-            datasette.urls.static_plugins(
-                "datasette_show_table",
-                "show-table.js",
+            datasette.static(
+                "show-table.js", plugin="datasette_show_table"
             )
         ]
 
diff --git a/docs/template_context.rst b/docs/template_context.rst
index 52ccca49..5c6b1567 100644
--- a/docs/template_context.rst
+++ b/docs/template_context.rst
@@ -47,15 +47,6 @@ These variables are available on every page rendered by Datasette, including pag
 ``show_logout``
     True if the logout link should be shown in the navigation menu
 
-``app_css_hash``
-    Hash of Datasette's app.css contents, used for cache busting
-
-``edit_tools_js_hash``
-    Hash of Datasette's edit-tools.js contents, used for cache busting
-
-``table_js_hash``
-    Hash of Datasette's table.js contents, used for cache busting
-
 ``zip``
     Python's ``zip()`` builtin, made available to template logic
 
diff --git a/docs/writing_plugins.rst b/docs/writing_plugins.rst
index cd165a3f..d1e5e75a 100644
--- a/docs/writing_plugins.rst
+++ b/docs/writing_plugins.rst
@@ -145,7 +145,16 @@ If your plugin has a ``static/`` directory, Datasette will automatically configu
 
     /-/static-plugins/NAME_OF_PLUGIN_PACKAGE/yourfile.js
 
-Use the ``datasette.urls.static_plugins(plugin_name, path)`` method to generate URLs to that asset that take the ``base_url`` setting into account, see :ref:`internals_datasette_urls`.
+Use the ``datasette.static(path, plugin=plugin_name)`` method to generate
+cache-busting URLs to those assets that take the ``base_url`` setting into
+account, see :ref:`datasette_static`.
+
+This can also be used from plugin templates as the ``static()`` template
+function:
+
+.. code-block:: html+jinja
+
+    <script src="{{ static('plugin.js', plugin='datasette_plugin_name') }}" defer></script>
 
 To bundle the static assets for a plugin in the package that you publish to PyPI, add the following to the plugin's ``setup.py``:
 
diff --git a/tests/test_html.py b/tests/test_html.py
index 20ab22bc..22943300 100644
--- a/tests/test_html.py
+++ b/tests/test_html.py
@@ -4,6 +4,7 @@ from datasette.utils import allowed_pragmas
 from .fixtures import make_app_client
 from .utils import assert_footer_links, inner_html
 import copy
+import hashlib
 import json
 import pathlib
 import pytest
@@ -83,7 +84,7 @@ async def test_homepage_options(ds_client):
 async def test_favicon(ds_client):
     response = await ds_client.get("/favicon.ico")
     assert response.status_code == 200
-    assert response.headers["cache-control"] == "max-age=3600, immutable, public"
+    assert response.headers["cache-control"] == "max-age=3600, public"
     assert int(response.headers["content-length"]) > 100
     assert response.headers["content-type"] == "image/png"
 
@@ -101,6 +102,24 @@ async def test_static(ds_client):
     assert response.status_code == 304
 
 
+@pytest.mark.asyncio
+async def test_static_hash_cache_control(ds_client):
+    hashed_url = ds_client.ds.static("app.css")
+    response = await ds_client.get(hashed_url)
+    assert response.status_code == 200
+    assert response.headers["cache-control"] == "max-age=31536000, immutable, public"
+
+    response = await ds_client.get(
+        hashed_url, headers={"if-none-match": response.headers["etag"]}
+    )
+    assert response.status_code == 304
+    assert response.headers["cache-control"] == "max-age=31536000, immutable, public"
+
+    response = await ds_client.get("/-/static/app.css?_hash=incorrect")
+    assert response.status_code == 200
+    assert "cache-control" not in response.headers
+
+
 def test_static_mounts():
     with make_app_client(
         static_mounts=[("custom-static", str(pathlib.Path(__file__).parent))]
@@ -113,6 +132,23 @@ def test_static_mounts():
         assert response.status_code == 404
 
 
+def test_static_mounts_hash_cache_control():
+    mount_path = pathlib.Path(__file__).parent
+    with make_app_client(static_mounts=[("custom-static", str(mount_path))]) as client:
+        response = client.get(client.ds.static("test_html.py", mount="custom-static"))
+        assert response.status_code == 200
+        assert (
+            response.headers["cache-control"] == "max-age=31536000, immutable, public"
+        )
+
+        incorrect_hash = hashlib.sha256(b"incorrect").hexdigest()[:12]
+        response = client.get(
+            "/custom-static/test_html.py?_hash={}".format(incorrect_hash)
+        )
+        assert response.status_code == 200
+        assert "cache-control" not in response.headers
+
+
 def test_memory_database_page():
     with make_app_client(memory=True) as client:
         response = client.get("/_memory")
@@ -609,7 +645,7 @@ async def test_404(ds_client, path):
     response = await ds_client.get(path)
     assert response.status_code == 404
     assert (
-        f'<link rel="stylesheet" href="/-/static/app.css?{ds_client.ds.app_css_hash()}'
+        '<link rel="stylesheet" href="{}"'.format(ds_client.ds.static("app.css"))
         in response.text
     )
 
@@ -1082,7 +1118,9 @@ async def test_navigation_menu_links(
     navigation_search_script = soup.find(
         "script", {"src": re.compile(r"navigation-search\.js")}
     )
-    assert navigation_search_script["src"] == "/-/static/navigation-search.js"
+    assert navigation_search_script["src"] == ds_client.ds.static(
+        "navigation-search.js"
+    )
     assert details.find("li").find("button") == search_button
     if not actor_id:
         # The app menu is always visible, but anonymous users do not see logout
diff --git a/tests/test_internals_datasette.py b/tests/test_internals_datasette.py
index e9c78ecc..2eaee3f9 100644
--- a/tests/test_internals_datasette.py
+++ b/tests/test_internals_datasette.py
@@ -4,6 +4,8 @@ Tests for the datasette.app.Datasette class
 
 import asyncio
 import dataclasses
+import hashlib
+import importlib
 import os
 import sqlite3
 import time
@@ -11,6 +13,7 @@ from datasette import Context
 from datasette.app import Datasette, Database, ResourcesSQL
 from datasette.database import DatasetteClosedError
 from datasette.resources import DatabaseResource
+from datasette.utils import PrefixedUrlString
 from itsdangerous import BadSignature
 import pytest
 
@@ -56,6 +59,111 @@ def test_datasette_setting(datasette, setting, expected):
     assert datasette.setting(setting) == expected
 
 
+def _setup_static_app_root(tmp_path, monkeypatch, filename, content):
+    app_module = importlib.import_module("datasette.app")
+    app_root = tmp_path / "app-root"
+    static_path = app_root / "datasette" / "static"
+    static_path.mkdir(parents=True)
+    asset_path = static_path / filename
+    asset_path.write_bytes(content)
+    monkeypatch.setattr(app_module, "app_root", app_root)
+    return asset_path
+
+
+@pytest.mark.asyncio
+async def test_static_template_function_hashes_core_asset(tmp_path, monkeypatch):
+    _setup_static_app_root(tmp_path, monkeypatch, "demo.js", b"const demo = true;")
+    ds = Datasette()
+    template = ds.get_jinja_environment().from_string("{{ static('demo.js') }}")
+    expected_hash = hashlib.sha256(b"const demo = true;").hexdigest()[:12]
+
+    assert await template.render_async() == "/-/static/demo.js?_hash={}".format(
+        expected_hash
+    )
+    assert isinstance(ds.static("demo.js"), PrefixedUrlString)
+
+
+def test_static_hash_cached_when_cache_headers_enabled(tmp_path, monkeypatch):
+    asset_path = _setup_static_app_root(tmp_path, monkeypatch, "demo.js", b"let a = 1;")
+    ds = Datasette(cache_headers=True)
+    first_url = ds.static("demo.js")
+
+    asset_path.write_bytes(b"let a = 2;")
+
+    assert ds.static("demo.js") == first_url
+
+
+def test_static_hash_recalculated_when_cache_headers_disabled(tmp_path, monkeypatch):
+    asset_path = _setup_static_app_root(tmp_path, monkeypatch, "demo.js", b"let a = 1;")
+    ds = Datasette(cache_headers=False)
+    first_url = ds.static("demo.js")
+
+    asset_path.write_bytes(b"let a = 2;")
+
+    expected_hash = hashlib.sha256(b"let a = 2;").hexdigest()[:12]
+    assert ds.static("demo.js") == "/-/static/demo.js?_hash={}".format(expected_hash)
+    assert ds.static("demo.js") != first_url
+
+
+def test_static_hashes_mounted_static_file(tmp_path):
+    static_path = tmp_path / "static-files"
+    static_path.mkdir()
+    asset_path = static_path / "styles.css"
+    asset_path.write_bytes(b"body { color: black; }")
+    ds = Datasette(static_mounts=[("assets", str(static_path))])
+    expected_hash = hashlib.sha256(b"body { color: black; }").hexdigest()[:12]
+
+    assert ds.static("styles.css", mount="assets") == (
+        "/assets/styles.css?_hash={}".format(expected_hash)
+    )
+
+    ds._settings["base_url"] = "/prefix/"
+    assert ds.static("styles.css", mount="assets") == (
+        "/prefix/assets/styles.css?_hash={}".format(expected_hash)
+    )
+
+
+def test_static_hashes_plugin_static_file(tmp_path, monkeypatch):
+    plugin_static_path = tmp_path / "plugin-static"
+    plugin_static_path.mkdir()
+    asset_path = plugin_static_path / "plugin.js"
+    asset_path.write_bytes(b"console.log('plugin');")
+    app_module = importlib.import_module("datasette.app")
+    monkeypatch.setattr(
+        app_module,
+        "get_plugins",
+        lambda: [
+            {
+                "name": "datasette-cluster-map",
+                "static_path": str(plugin_static_path),
+                "templates_path": None,
+            }
+        ],
+    )
+    ds = Datasette()
+    expected_hash = hashlib.sha256(b"console.log('plugin');").hexdigest()[:12]
+
+    assert ds.static("plugin.js", plugin="datasette_cluster_map") == (
+        "/-/static-plugins/datasette_cluster_map/plugin.js?_hash={}".format(
+            expected_hash
+        )
+    )
+
+
+def test_static_rejects_plugin_and_mount():
+    ds = Datasette()
+    with pytest.raises(ValueError):
+        ds.static("styles.css", plugin="datasette_cluster_map", mount="assets")
+
+
+def test_static_rejects_path_traversal(tmp_path, monkeypatch):
+    _setup_static_app_root(tmp_path, monkeypatch, "demo.js", b"")
+    ds = Datasette()
+
+    with pytest.raises(ValueError, match="cannot escape static root"):
+        ds.static("../secret.js")
+
+
 @pytest.mark.asyncio
 async def test_datasette_constructor():
     ds = Datasette()
diff --git a/tests/test_utils.py b/tests/test_utils.py
index 74f1963f..8d080a8a 100644
--- a/tests/test_utils.py
+++ b/tests/test_utils.py
@@ -11,6 +11,7 @@ from datasette.utils.sqlite import (
     sqlite_table_type,
     supports_returning,
 )
+import hashlib
 import json
 import os
 import pathlib
@@ -835,6 +836,12 @@ def test_pairs_to_nested_config(pairs, expected):
     assert actual == expected
 
 
+def test_sha256_file(tmp_path):
+    path = tmp_path / "test.txt"
+    path.write_text("hello")
+    assert utils.sha256_file(path, chunk_size=2) == hashlib.sha256(b"hello").hexdigest()
+
+
 @pytest.mark.asyncio
 async def test_calculate_etag(tmp_path):
     path = tmp_path / "test.txt"