diff --git a/lib/pleroma/plugs/frontend_static.ex b/lib/pleroma/plugs/frontend_static.ex
new file mode 100644
index 000000000..f549ca75f
--- /dev/null
+++ b/lib/pleroma/plugs/frontend_static.ex
@@ -0,0 +1,54 @@
+# Pleroma: A lightweight social networking server
+# Copyright © 2017-2020 Pleroma Authors <https://pleroma.social/>
+# SPDX-License-Identifier: AGPL-3.0-only
+
+defmodule Pleroma.Plugs.FrontendStatic do
+  require Pleroma.Constants
+
+  @moduledoc """
+  This is a shim to call `Plug.Static` but with runtime `from` configuration`. It dispatches to the different frontends.
+  """
+  @behaviour Plug
+
+  def file_path(path, frontend_type \\ :primary) do
+    if configuration = Pleroma.Config.get([:frontends, frontend_type]) do
+      instance_static_path = Pleroma.Config.get([:instance, :static_dir], "instance/static")
+
+      Path.join([
+        instance_static_path,
+        "frontends",
+        configuration["name"],
+        configuration["ref"],
+        path
+      ])
+    else
+      nil
+    end
+  end
+
+  def init(opts) do
+    opts
+    |> Keyword.put(:from, "__unconfigured_frontend_static_plug")
+    |> Plug.Static.init()
+  end
+
+  def call(conn, opts) do
+    frontend_type = Map.get(opts, :frontend_type, :primary)
+    path = file_path("", frontend_type)
+
+    if path do
+      conn
+      |> call_static(opts, path)
+    else
+      conn
+    end
+  end
+
+  defp call_static(conn, opts, from) do
+    opts =
+      opts
+      |> Map.put(:from, from)
+
+    Plug.Static.call(conn, opts)
+  end
+end
diff --git a/lib/pleroma/plugs/instance_static.ex b/lib/pleroma/plugs/instance_static.ex
index 18255eac3..0fb57e422 100644
--- a/lib/pleroma/plugs/instance_static.ex
+++ b/lib/pleroma/plugs/instance_static.ex
@@ -16,11 +16,11 @@ def file_path(path) do
     instance_path =
       Path.join(Pleroma.Config.get([:instance, :static_dir], "instance/static/"), path)
 
-    if File.exists?(instance_path) do
-      instance_path
-    else
+    frontend_path = Pleroma.Plugs.FrontendStatic.file_path(path, :primary)
+
+    (File.exists?(instance_path) && instance_path) ||
+      (frontend_path && File.exists?(frontend_path) && frontend_path) ||
       Path.join(Application.app_dir(:pleroma, "priv/static/"), path)
-    end
   end
 
   def init(opts) do
diff --git a/lib/pleroma/web/endpoint.ex b/lib/pleroma/web/endpoint.ex
index 226d42c2c..527fb288d 100644
--- a/lib/pleroma/web/endpoint.ex
+++ b/lib/pleroma/web/endpoint.ex
@@ -28,6 +28,17 @@ defmodule Pleroma.Web.Endpoint do
     }
   )
 
+  # Careful! No `only` restriction here, as we don't know what frontends contain.
+  plug(Pleroma.Plugs.FrontendStatic,
+    at: "/",
+    frontend_type: :primary,
+    gzip: true,
+    cache_control_for_etags: @static_cache_control,
+    headers: %{
+      "cache-control" => @static_cache_control
+    }
+  )
+
   # Serve at "/" the static files from "priv/static" directory.
   #
   # You should set gzip to true if you are running phoenix.digest
diff --git a/test/plugs/frontend_static_test.exs b/test/plugs/frontend_static_test.exs
new file mode 100644
index 000000000..d11d91d78
--- /dev/null
+++ b/test/plugs/frontend_static_test.exs
@@ -0,0 +1,30 @@
+# Pleroma: A lightweight social networking server
+# Copyright © 2017-2020 Pleroma Authors <https://pleroma.social/>
+# SPDX-License-Identifier: AGPL-3.0-only
+
+defmodule Pleroma.Web.FrontendStaticPlugTest do
+  use Pleroma.Web.ConnCase
+
+  @dir "test/tmp/instance_static"
+
+  setup do
+    File.mkdir_p!(@dir)
+    on_exit(fn -> File.rm_rf(@dir) end)
+  end
+
+  setup do: clear_config([:instance, :static_dir], @dir)
+
+  test "overrides existing static files", %{conn: conn} do
+    name = "pelmora"
+    ref = "uguu"
+
+    clear_config([:frontends, :primary], %{"name" => name, "ref" => ref})
+    path = "#{@dir}/frontends/#{name}/#{ref}"
+
+    File.mkdir_p!(path)
+    File.write!("#{path}/index.html", "from frontend plug")
+
+    index = get(conn, "/")
+    assert html_response(index, 200) == "from frontend plug"
+  end
+end
diff --git a/test/plugs/instance_static_test.exs b/test/plugs/instance_static_test.exs
index be2613ad0..d42ba817e 100644
--- a/test/plugs/instance_static_test.exs
+++ b/test/plugs/instance_static_test.exs
@@ -2,7 +2,7 @@
 # Copyright © 2017-2020 Pleroma Authors <https://pleroma.social/>
 # SPDX-License-Identifier: AGPL-3.0-only
 
-defmodule Pleroma.Web.RuntimeStaticPlugTest do
+defmodule Pleroma.Web.InstanceStaticPlugTest do
   use Pleroma.Web.ConnCase
 
   @dir "test/tmp/instance_static"
@@ -24,6 +24,28 @@ test "overrides index" do
     assert html_response(index, 200) == "hello world"
   end
 
+  test "also overrides frontend files", %{conn: conn} do
+    name = "pelmora"
+    ref = "uguu"
+
+    clear_config([:frontends, :primary], %{"name" => name, "ref" => ref})
+
+    bundled_index = get(conn, "/")
+    refute html_response(bundled_index, 200) == "from frontend plug"
+
+    path = "#{@dir}/frontends/#{name}/#{ref}"
+    File.mkdir_p!(path)
+    File.write!("#{path}/index.html", "from frontend plug")
+
+    index = get(conn, "/")
+    assert html_response(index, 200) == "from frontend plug"
+
+    File.write!(@dir <> "/index.html", "from instance static")
+
+    index = get(conn, "/")
+    assert html_response(index, 200) == "from instance static"
+  end
+
   test "overrides any file in static/static" do
     bundled_index = get(build_conn(), "/static/terms-of-service.html")