diff --git a/lib/livebook/session.ex b/lib/livebook/session.ex
index fdb8395920e..1012294f495 100644
--- a/lib/livebook/session.ex
+++ b/lib/livebook/session.ex
@@ -222,6 +222,16 @@ defmodule Livebook.Session do
     GenServer.call(pid, {:register_client, client_pid, user}, @timeout)
   end
 
+  @doc """
+  Resets the auto shutdown timer, if ticking.
+
+  When the session has connected clients, nothing changes.
+  """
+  @spec reset_auto_shutdown(pid()) :: :ok
+  def reset_auto_shutdown(pid) do
+    GenServer.cast(pid, :reset_auto_shutdown)
+  end
+
   @doc """
   Returns data of the given session.
   """
@@ -959,25 +969,31 @@ defmodule Livebook.Session do
   defp schedule_auto_shutdown(state) do
     client_count = map_size(state.data.clients_map)
 
-    case {client_count, state.auto_shutdown_timer_ref} do
-      {0, nil} when state.auto_shutdown_ms != nil ->
+    cond do
+      client_count == 0 and state.auto_shutdown_timer_ref == nil and state.auto_shutdown_ms != nil ->
         timer_ref = Process.send_after(self(), :close, state.auto_shutdown_ms)
         %{state | auto_shutdown_timer_ref: timer_ref}
 
-      {client_count, timer_ref} when client_count > 0 and timer_ref != nil ->
-        if Process.cancel_timer(timer_ref) == false do
-          receive do
-            :close -> :ok
-          end
-        end
-
-        %{state | auto_shutdown_timer_ref: nil}
+      client_count > 0 ->
+        cancel_auto_shutdown_timer(state)
 
-      _ ->
+      true ->
         state
     end
   end
 
+  defp cancel_auto_shutdown_timer(%{auto_shutdown_timer_ref: nil} = state), do: state
+
+  defp cancel_auto_shutdown_timer(state) do
+    if Process.cancel_timer(state.auto_shutdown_timer_ref) == false do
+      receive do
+        :close -> :ok
+      end
+    end
+
+    %{state | auto_shutdown_timer_ref: nil}
+  end
+
   @impl true
   def handle_continue(:app_init, state) do
     cell_ids = Data.cell_ids_for_full_evaluation(state.data, [])
@@ -1091,6 +1107,13 @@ defmodule Livebook.Session do
   end
 
   @impl true
+  def handle_cast(:reset_auto_shutdown, state) do
+    {:noreply,
+     state
+     |> cancel_auto_shutdown_timer()
+     |> schedule_auto_shutdown()}
+  end
+
   def handle_cast({:set_notebook_attributes, client_pid, attrs}, state) do
     client_id = client_id(state, client_pid)
     operation = {:set_notebook_attributes, client_id, attrs}
@@ -2466,7 +2489,7 @@ defmodule Livebook.Session do
     status = state.data.app_data.status
     send(state.app_pid, {:app_status_changed, state.session_id, status})
 
-    notify_update(state)
+    state
   end
 
   defp handle_action(state, :app_recover) do
diff --git a/lib/livebook_web/errors.ex b/lib/livebook_web/errors.ex
new file mode 100644
index 00000000000..11f6326c771
--- /dev/null
+++ b/lib/livebook_web/errors.ex
@@ -0,0 +1,7 @@
+defmodule LivebookWeb.NotFoundError do
+  defexception [:message, plug_status: 404]
+end
+
+defmodule LivebookWeb.BadRequestError do
+  defexception [:message, plug_status: 400]
+end
diff --git a/lib/livebook_web/errors/not_found_error.ex b/lib/livebook_web/errors/not_found_error.ex
deleted file mode 100644
index 414880c2ec0..00000000000
--- a/lib/livebook_web/errors/not_found_error.ex
+++ /dev/null
@@ -1,3 +0,0 @@
-defmodule LivebookWeb.NotFoundError do
-  defexception [:message, plug_status: 404]
-end
diff --git a/lib/livebook_web/plugs/proxy_plug.ex b/lib/livebook_web/plugs/proxy_plug.ex
index 5f1d266c0fd..4491be81660 100644
--- a/lib/livebook_web/plugs/proxy_plug.ex
+++ b/lib/livebook_web/plugs/proxy_plug.ex
@@ -11,24 +11,43 @@ defmodule LivebookWeb.ProxyPlug do
   @impl true
   def call(%{path_info: ["sessions", id, "proxy" | path_info]} = conn, _opts) do
     session = fetch_session!(id)
+    Livebook.Session.reset_auto_shutdown(session.pid)
     proxy_handler_spec = fetch_proxy_handler_spec!(session)
     conn = prepare_conn(conn, path_info, ["sessions", id, "proxy"])
-    conn = call_proxy_handler(proxy_handler_spec, conn)
-    halt(conn)
+    call_proxy_handler(proxy_handler_spec, conn)
   end
 
   def call(%{path_info: ["apps", slug, id, "proxy" | path_info]} = conn, _opts) do
     app = fetch_app!(slug)
 
     unless Enum.any?(app.sessions, &(&1.id == id)) do
-      raise NotFoundError, "could not find an app session matching #{inspect(id)}"
+      raise NotFoundError, "could not find an app session with id #{inspect(id)}"
     end
 
     session = fetch_session!(id)
+    Livebook.Session.reset_auto_shutdown(session.pid)
+    await_app_session_ready(app, session.id)
+    proxy_handler_spec = fetch_proxy_handler_spec!(session)
+    conn = prepare_conn(conn, path_info, ["apps", slug, id, "proxy"])
+    call_proxy_handler(proxy_handler_spec, conn)
+  end
+
+  def call(%{path_info: ["apps", slug, "proxy" | path_info]} = conn, _opts) do
+    app = fetch_app!(slug)
+
+    if app.multi_session do
+      raise LivebookWeb.BadRequestError,
+            "the requested app is multi-session. In order to send requests to this app," <>
+              " you need to start a session and use its specific URL"
+    end
+
+    session_id = Livebook.App.get_session_id(app.pid)
+    {:ok, session} = Livebook.Sessions.fetch_session(session_id)
+    Livebook.Session.reset_auto_shutdown(session.pid)
+    await_app_session_ready(app, session.id)
     proxy_handler_spec = fetch_proxy_handler_spec!(session)
     conn = prepare_conn(conn, path_info, ["apps", slug, "proxy"])
-    conn = call_proxy_handler(proxy_handler_spec, conn)
-    halt(conn)
+    call_proxy_handler(proxy_handler_spec, conn)
   end
 
   def call(conn, _opts) do
@@ -38,21 +57,27 @@ defmodule LivebookWeb.ProxyPlug do
   defp fetch_app!(slug) do
     case Livebook.Apps.fetch_app(slug) do
       {:ok, app} -> app
-      :error -> raise NotFoundError, "could not find an app matching #{inspect(slug)}"
+      :error -> raise NotFoundError, "could not find an app with slug #{inspect(slug)}"
     end
   end
 
   defp fetch_session!(id) do
     case Livebook.Sessions.fetch_session(id) do
       {:ok, session} -> session
-      {:error, _} -> raise NotFoundError, "could not find a session matching #{id}"
+      {:error, _} -> raise NotFoundError, "could not find a session with id #{id}"
     end
   end
 
   defp fetch_proxy_handler_spec!(session) do
     case Livebook.Session.fetch_proxy_handler_spec(session.pid) do
-      {:ok, pid} -> pid
-      {:error, _} -> raise NotFoundError, "could not find a kino proxy running"
+      {:ok, pid} ->
+        pid
+
+      {:error, _} ->
+        raise NotFoundError,
+              "the session does not listen to proxied requests." <>
+                " See the Kino.Proxy documentation to learn about defining" <>
+                " custom request handlers"
     end
   end
 
@@ -62,6 +87,32 @@ defmodule LivebookWeb.ProxyPlug do
 
   defp call_proxy_handler(proxy_handler_spec, conn) do
     {module, function, args} = proxy_handler_spec
-    apply(module, function, args ++ [conn])
+    conn = apply(module, function, args ++ [conn])
+    halt(conn)
+  end
+
+  defp await_app_session_ready(app, session_id) do
+    unless session_ready?(app, session_id) do
+      Livebook.App.subscribe(app.slug)
+      await_session_execution_loop(app, session_id)
+      Livebook.App.unsubscribe(app.slug)
+    end
+  end
+
+  defp await_session_execution_loop(%{slug: slug}, session_id) do
+    receive do
+      {:app_updated, %{slug: ^slug} = app} ->
+        unless session_ready?(app, session_id) do
+          await_session_execution_loop(app, session_id)
+        end
+    end
+  end
+
+  defp session_ready?(app, session_id) do
+    if session = Enum.find(app.sessions, &(&1.id == session_id)) do
+      session.app_status.execution != :executing
+    else
+      false
+    end
   end
 end
diff --git a/test/livebook/proxy_test.exs b/test/livebook/proxy_test.exs
index ae533db415f..71056e8fd4e 100644
--- a/test/livebook/proxy_test.exs
+++ b/test/livebook/proxy_test.exs
@@ -78,6 +78,58 @@ defmodule Livebook.ProxyTest do
       assert text_response(put(conn, url), 200) == "used PUT method"
       assert text_response(patch(conn, url), 200) == "used PATCH method"
       assert text_response(delete(conn, url), 200) == "used DELETE method"
+
+      # Generic path also works for single-session apps
+      url = "/apps/#{slug}/proxy/"
+
+      assert text_response(get(conn, url), 200) == "used GET method"
+    end
+
+    test "waits for the session to be executed before attempting the request", %{conn: conn} do
+      slug = Livebook.Utils.random_short_id()
+
+      app_settings = %{
+        Notebook.AppSettings.new()
+        | slug: slug,
+          access_type: :public,
+          auto_shutdown_ms: 5_000
+      }
+
+      notebook = %{proxy_notebook() | app_settings: app_settings}
+
+      Livebook.Apps.subscribe()
+      pid = deploy_notebook_sync(notebook)
+
+      assert_receive {:app_created, %{pid: ^pid, slug: ^slug, sessions: []}}
+
+      # The app is configured with auto shutdown, so the session will
+      # start only once requested. We should wait until it executes
+      # and then proxy the request as usual
+      url = "/apps/#{slug}/proxy/"
+
+      assert text_response(get(conn, url), 200) == "used GET method"
+    end
+
+    test "returns error when requesting generic path for multi-session app", %{conn: conn} do
+      slug = Livebook.Utils.random_short_id()
+
+      app_settings = %{
+        Notebook.AppSettings.new()
+        | slug: slug,
+          access_type: :public,
+          multi_session: true
+      }
+
+      notebook = %{proxy_notebook() | app_settings: app_settings}
+
+      Livebook.Apps.subscribe()
+      pid = deploy_notebook_sync(notebook)
+
+      assert_receive {:app_created, %{pid: ^pid, slug: ^slug, sessions: []}}
+
+      assert_error_sent 400, fn ->
+        get(conn, "/apps/#{slug}/proxy/foo/bar")
+      end
     end
   end