diff --git a/assets/js/hooks/js_view.js b/assets/js/hooks/js_view.js
index 8a0b4b301..f619a10df 100644
--- a/assets/js/hooks/js_view.js
+++ b/assets/js/hooks/js_view.js
@@ -364,12 +364,6 @@ const JSView = {
           preselect_name: message.preselectName,
           options: message.options,
         });
-      } else if (message.type === "setSmartCellEditorIntellisenseNode") {
-        this.pushEvent("set_smart_cell_editor_intellisense_node", {
-          js_view_ref: this.props.ref,
-          node: message.node,
-          cookie: message.cookie,
-        });
       }
     }
   },
diff --git a/lib/livebook/notebook/cell/smart.ex b/lib/livebook/notebook/cell/smart.ex
index 74f34b1fa..ea44f05a4 100644
--- a/lib/livebook/notebook/cell/smart.ex
+++ b/lib/livebook/notebook/cell/smart.ex
@@ -18,8 +18,7 @@ defmodule Livebook.Notebook.Cell.Smart do
     :kind,
     :attrs,
     :js_view,
-    :editor,
-    :editor_intellisense_node
+    :editor
   ]
 
   alias Livebook.Utils
@@ -33,8 +32,7 @@ defmodule Livebook.Notebook.Cell.Smart do
           kind: String.t() | nil,
           attrs: attrs() | :__pruned__,
           js_view: Livebook.Runtime.js_view() | nil,
-          editor: Livebook.Runtime.editor() | nil,
-          editor_intellisense_node: {String.t(), String.t()} | nil
+          editor: Livebook.Runtime.editor() | nil
         }
 
   @type attrs :: map()
@@ -52,8 +50,7 @@ defmodule Livebook.Notebook.Cell.Smart do
       kind: nil,
       attrs: %{},
       js_view: nil,
-      editor: nil,
-      editor_intellisense_node: nil
+      editor: nil
     }
   end
 end
diff --git a/lib/livebook/runtime.ex b/lib/livebook/runtime.ex
index c8b31c964..eb5e162a7 100644
--- a/lib/livebook/runtime.ex
+++ b/lib/livebook/runtime.ex
@@ -704,7 +704,12 @@ defprotocol Livebook.Runtime do
   @typedoc """
   Smart cell editor configuration.
   """
-  @type editor :: %{language: String.t() | nil, placement: :bottom | :top, source: String.t()}
+  @type editor :: %{
+          language: String.t() | nil,
+          placement: :bottom | :top,
+          source: String.t(),
+          intellisense_node: {atom(), atom()} | nil
+        }
 
   @typedoc """
   An opaque file reference.
@@ -876,7 +881,7 @@ defprotocol Livebook.Runtime do
           pid(),
           intellisense_request(),
           parent_locators(),
-          {String.t(), String.t()} | nil
+          {atom(), atom()} | nil
         ) :: reference()
   def handle_intellisense(runtime, send_to, request, parent_locators, node)
 
@@ -945,6 +950,17 @@ defprotocol Livebook.Runtime do
   The attrs are persisted and may be used to restore the smart cell
   state later. Note that for persistence they get serialized and
   deserialized as JSON.
+
+  When the smart cell editor is enabled, the runtime owner sends the
+  new editor source whenever it changes as:
+
+    * `{:editor_source, source :: String.t()}`
+
+  The cell can also update some of the editor configuration or source
+  by sending:
+
+    * `{:runtime_smart_cell_editor_update, ref, %{optional(:source) => String.t(), optional(:intellisense_node) => {atom(), atom()} | nil}}`
+
   """
   @spec start_smart_cell(
           t(),
diff --git a/lib/livebook/runtime/erl_dist/runtime_server.ex b/lib/livebook/runtime/erl_dist/runtime_server.ex
index acdd0f07b..b0a624235 100644
--- a/lib/livebook/runtime/erl_dist/runtime_server.ex
+++ b/lib/livebook/runtime/erl_dist/runtime_server.ex
@@ -130,7 +130,7 @@ defmodule Livebook.Runtime.ErlDist.RuntimeServer do
           pid(),
           Runtime.intellisense_request(),
           Runtime.Runtime.parent_locators(),
-          {String.t(), String.t()} | nil
+          {atom(), atom()} | nil
         ) :: reference()
   def handle_intellisense(pid, send_to, request, parent_locators, node) do
     ref = make_ref()
@@ -921,7 +921,6 @@ defmodule Livebook.Runtime.ErlDist.RuntimeServer do
   end
 
   defp intellisense_node({node, cookie}) do
-    {node, cookie} = {String.to_atom(node), String.to_atom(cookie)}
     Node.set_cookie(node, cookie)
     if Node.connect(node), do: node, else: node()
   end
diff --git a/lib/livebook/session.ex b/lib/livebook/session.ex
index 794715795..fffc2daba 100644
--- a/lib/livebook/session.ex
+++ b/lib/livebook/session.ex
@@ -1661,6 +1661,8 @@ defmodule Livebook.Session do
   end
 
   def handle_info({:runtime_smart_cell_started, id, info}, state) do
+    info = normalize_smart_cell_started_info(info)
+
     info =
       if info.editor do
         normalize_newlines = &String.replace(&1, "\r\n", "\n")
@@ -1672,11 +1674,10 @@ defmodule Livebook.Session do
 
     case Notebook.fetch_cell_and_section(state.data.notebook, id) do
       {:ok, cell, _section} ->
-        chunks = info[:chunks]
         delta = Livebook.Text.Delta.diff(cell.source, info.source)
 
         operation =
-          {:smart_cell_started, @client_id, id, delta, chunks, info.js_view, info.editor}
+          {:smart_cell_started, @client_id, id, delta, info.chunks, info.js_view, info.editor}
 
         {:noreply, handle_operation(state, operation)}
 
@@ -1714,6 +1715,42 @@ defmodule Livebook.Session do
     end
   end
 
+  def handle_info({:runtime_smart_cell_editor_update, id, options}, state) do
+    case Notebook.fetch_cell_and_section(state.data.notebook, id) do
+      {:ok, cell, _section} when cell.editor != nil ->
+        state =
+          case options do
+            %{source: source} ->
+              delta = Livebook.Text.Delta.diff(cell.editor.source, source)
+              revision = state.data.cell_infos[cell.id].sources.secondary.revision
+
+              operation =
+                {:apply_cell_delta, @client_id, cell.id, :secondary, delta, nil, revision}
+
+              handle_operation(state, operation)
+
+            %{} ->
+              state
+          end
+
+        state =
+          case options do
+            %{intellisense_node: intellisense_node} ->
+              editor = %{cell.editor | intellisense_node: intellisense_node}
+              operation = {:set_cell_attributes, @client_id, cell.id, %{editor: editor}}
+              handle_operation(state, operation)
+
+            %{} ->
+              state
+          end
+
+        {:noreply, state}
+
+      _ ->
+        {:noreply, state}
+    end
+  end
+
   def handle_info({:pong, {:smart_cell_evaluation, cell_id}, _info}, state) do
     state =
       with {:ok, cell, section} <- Notebook.fetch_cell_and_section(state.data.notebook, cell_id),
@@ -3070,4 +3107,17 @@ defmodule Livebook.Session do
     %{type: :unknown, output: other}
     |> normalize_runtime_output()
   end
+
+  # Normalizes :runtime_smart_cell_started info to match the latest
+  # specification.
+  defp normalize_smart_cell_started_info(info) when not is_map_key(info, :chunks) do
+    normalize_smart_cell_started_info(put_in(info[:chunks], nil))
+  end
+
+  defp normalize_smart_cell_started_info(info)
+       when info.editor != nil and not is_map_key(info.editor, :intellisense_node) do
+    normalize_smart_cell_started_info(put_in(info.editor[:intellisense_node], nil))
+  end
+
+  defp normalize_smart_cell_started_info(info), do: info
 end
diff --git a/lib/livebook_web/live/session_live.ex b/lib/livebook_web/live/session_live.ex
index 89603037d..270226a01 100644
--- a/lib/livebook_web/live/session_live.ex
+++ b/lib/livebook_web/live/session_live.ex
@@ -858,23 +858,6 @@ defmodule LivebookWeb.SessionLive do
      push_patch(socket, to: ~p"/sessions/#{socket.assigns.session.id}/settings/custom-view")}
   end
 
-  def handle_event(
-        "set_smart_cell_editor_intellisense_node",
-        %{"js_view_ref" => cell_id, "node" => node, "cookie" => cookie},
-        socket
-      ) do
-    node =
-      if is_binary(node) and node =~ "@" and is_binary(cookie) and cookie != "" do
-        {node, cookie}
-      end
-
-    Session.set_cell_attributes(socket.assigns.session.pid, cell_id, %{
-      editor_intellisense_node: node
-    })
-
-    {:noreply, socket}
-  end
-
   @impl true
   def handle_call({:get_input_value, input_id}, _from, socket) do
     reply =
@@ -2105,7 +2088,7 @@ defmodule LivebookWeb.SessionLive do
     "#{notebook_name} - Livebook"
   end
 
-  defp intellisense_node(%Cell.Smart{editor_intellisense_node: node_cookie}), do: node_cookie
+  defp intellisense_node(%Cell.Smart{editor: %{intellisense_node: node_cookie}}), do: node_cookie
   defp intellisense_node(_), do: nil
 
   defp any_stale_cell?(data) do
diff --git a/test/livebook/session_test.exs b/test/livebook/session_test.exs
index dafdd9adc..17d8a8b8b 100644
--- a/test/livebook/session_test.exs
+++ b/test/livebook/session_test.exs
@@ -1033,6 +1033,54 @@ defmodule Livebook.SessionTest do
              } = Session.get_data(session.pid)
     end
 
+    test "handles smart cell editor updates" do
+      smart_cell = %{Notebook.Cell.new(:smart) | kind: "text", source: ""}
+      notebook = %{Notebook.new() | sections: [%{Notebook.Section.new() | cells: [smart_cell]}]}
+      session = start_session(notebook: notebook)
+
+      runtime = connected_noop_runtime()
+      Session.set_runtime(session.pid, runtime)
+
+      send(
+        session.pid,
+        {:runtime_smart_cell_definitions,
+         [%{kind: "text", name: "Text", requirement_presets: []}]}
+      )
+
+      Session.subscribe(session.id)
+
+      editor = %{language: nil, placement: :bottom, source: "", intellisense_node: nil}
+
+      send(
+        session.pid,
+        {:runtime_smart_cell_started, smart_cell.id,
+         %{source: "1", js_view: %{pid: self(), ref: "ref"}, editor: editor}}
+      )
+
+      # Update editor source
+      send(
+        session.pid,
+        {:runtime_smart_cell_editor_update, smart_cell.id, %{source: "new source"}}
+      )
+
+      assert %{
+               notebook: %{sections: [%{cells: [%{editor: %{source: "new source"}}]}]}
+             } = Session.get_data(session.pid)
+
+      # Update intellisense node
+      send(
+        session.pid,
+        {:runtime_smart_cell_editor_update, smart_cell.id,
+         %{intellisense_node: {:test@test, :test}}}
+      )
+
+      assert %{
+               notebook: %{
+                 sections: [%{cells: [%{editor: %{intellisense_node: {:test@test, :test}}}]}]
+               }
+             } = Session.get_data(session.pid)
+    end
+
     test "pings the smart cell before evaluation to await all incoming messages" do
       smart_cell = %{Notebook.Cell.new(:smart) | kind: "text", source: ""}
       notebook = %{Notebook.new() | sections: [%{Notebook.Section.new() | cells: [smart_cell]}]}