diff --git a/lib/livebook/proxy/adapter.ex b/lib/livebook/proxy/adapter.ex
index 30c681a8a..d409e6074 100644
--- a/lib/livebook/proxy/adapter.ex
+++ b/lib/livebook/proxy/adapter.ex
@@ -1,7 +1,14 @@
 defmodule Livebook.Proxy.Adapter do
   @moduledoc false
+
+  # Implements a Plug adapter for handling `conn` within the runtime.
+  #
+  # All actions are forwarded to the parent process (`Livebook.Proxy.Server`),
+  # which operates within Livebook itself.
+
   @behaviour Plug.Conn.Adapter
 
+  @impl true
   def send_resp({pid, ref}, status, headers, body) do
     send(pid, {:send_resp, self(), ref, status, headers, body})
 
@@ -11,6 +18,7 @@ defmodule Livebook.Proxy.Adapter do
     end
   end
 
+  @impl true
   def get_peer_data({pid, ref}) do
     send(pid, {:get_peer_data, self(), ref})
 
@@ -20,6 +28,7 @@ defmodule Livebook.Proxy.Adapter do
     end
   end
 
+  @impl true
   def get_http_protocol({pid, ref}) do
     send(pid, {:get_http_protocol, self(), ref})
 
@@ -29,6 +38,7 @@ defmodule Livebook.Proxy.Adapter do
     end
   end
 
+  @impl true
   def read_req_body({pid, ref}, opts) do
     send(pid, {:read_req_body, self(), ref, opts})
 
@@ -40,6 +50,7 @@ defmodule Livebook.Proxy.Adapter do
     end
   end
 
+  @impl true
   def send_chunked({pid, ref}, status, headers) do
     send(pid, {:send_chunked, self(), ref, status, headers})
 
@@ -49,6 +60,7 @@ defmodule Livebook.Proxy.Adapter do
     end
   end
 
+  @impl true
   def chunk({pid, ref}, chunk) do
     send(pid, {:chunk, self(), ref, chunk})
 
@@ -59,6 +71,7 @@ defmodule Livebook.Proxy.Adapter do
     end
   end
 
+  @impl true
   def inform({pid, ref}, status, headers) do
     send(pid, {:inform, self(), ref, status, headers})
 
@@ -68,6 +81,7 @@ defmodule Livebook.Proxy.Adapter do
     end
   end
 
+  @impl true
   def send_file({pid, ref}, status, headers, path, offset, length) do
     %File.Stat{type: :regular, size: size} = File.stat!(path)
 
@@ -90,7 +104,10 @@ defmodule Livebook.Proxy.Adapter do
     end
   end
 
+  @impl true
   def upgrade(_payload, _protocol, _opts), do: {:error, :not_supported}
+
+  @impl true
   def push(_payload, _path, _headers), do: {:error, :not_supported}
 
   defp exit_fun(fun, arity, reason) do
diff --git a/lib/livebook/proxy/handler.ex b/lib/livebook/proxy/handler.ex
index fcef5411e..9475758b4 100644
--- a/lib/livebook/proxy/handler.ex
+++ b/lib/livebook/proxy/handler.ex
@@ -1,21 +1,58 @@
 defmodule Livebook.Proxy.Handler do
   @moduledoc false
 
+  # Handles request `conn` with the configured function.
+  #
+  # The handler forwards all actual communication to the parent
+  # `Livebook.Proxy.Server` via `Livebook.Proxy.Adapter`.
+  #
+  # A handler process is started on demand under a task supervisor.
+  # To avoid bottlenecks, we use a partition supervisor, so that we
+  # have a group of task supervisors ready.
+
+  @name __MODULE__
+
+  @doc """
+  Returns a child spec to setup the handler supervision tree.
+
+  Expects the `:listen` option to be provided, and be a function with
+  the signature `Plug.Conn.t() -> Plug.Conn.t()`.
+  """
+  @spec child_spec(keyword()) :: Supervisor.child_spec()
   def child_spec(opts) do
-    name = Keyword.fetch!(opts, :name)
     listen = Keyword.fetch!(opts, :listen)
-    :persistent_term.put({__MODULE__, name}, listen)
-    PartitionSupervisor.child_spec(child_spec: Task.Supervisor, name: name)
+    :persistent_term.put({__MODULE__, :listen}, listen)
+    PartitionSupervisor.child_spec(child_spec: Task.Supervisor, name: @name)
   end
 
-  def serve(parent, name, data) when is_pid(parent) and is_atom(name) do
-    Process.link(parent)
-    ref = Process.monitor(parent)
-    conn = struct!(Plug.Conn, %{data | adapter: {Livebook.Proxy.Adapter, {parent, ref}}})
-    :persistent_term.get({__MODULE__, name}).(conn)
+  @doc """
+  Handles request with the configured listener function.
+
+  Restores `%Plug.Conn{}` from the given attributes and delegates
+  all response handling back to the parent `Livebook.Proxy.Server`.
+  """
+  @spec serve(pid(), map()) :: Plug.Conn.t()
+  def serve(parent_pid, %{} = conn_attrs) when is_pid(parent_pid) do
+    Process.link(parent_pid)
+    ref = Process.monitor(parent_pid)
+
+    conn =
+      struct!(Plug.Conn, %{conn_attrs | adapter: {Livebook.Proxy.Adapter, {parent_pid, ref}}})
+
+    listen = :persistent_term.get({__MODULE__, :listen})
+    listen.(conn)
   end
 
-  def get_pid(name, key) do
-    GenServer.whereis({:via, PartitionSupervisor, {name, key}})
+  @doc """
+  Returns a pid of task supervisor to start the handler under.
+
+  In case no supervisor is running, returns `nil`.
+  """
+  @spec get_supervisor_pid() :: pid() | nil
+  def get_supervisor_pid() do
+    if Process.whereis(@name) do
+      key = :rand.uniform()
+      GenServer.whereis({:via, PartitionSupervisor, {@name, key}})
+    end
   end
 end
diff --git a/lib/livebook/proxy/server.ex b/lib/livebook/proxy/server.ex
index 5a0856e96..3cb1a300e 100644
--- a/lib/livebook/proxy/server.ex
+++ b/lib/livebook/proxy/server.ex
@@ -1,15 +1,39 @@
 defmodule Livebook.Proxy.Server do
   @moduledoc false
+
+  # The entrypoint for delegating `conn` handling to a runtime.
+  #
+  # The `Livebook.Proxy` modules are an implementation detail of the
+  # runtime. `Livebook.Proxy.Server` lives on the Livebook-side and
+  # it delegates request handling to `Livebook.Proxy.Handler`, which
+  # lives in the runtime node. The handler uses a custom plug adapter
+  # that dispatches `%Plug.Conn{}` operations as messages back to the
+  # server.
+  #
+  # Note that the server is not itself a new process, it is whoever
+  # calls `serve/2`.
+
   import Plug.Conn
 
-  def serve(pid, name, %Plug.Conn{} = conn) when is_pid(pid) and is_atom(name) do
-    args = [self(), name, build_client_conn(conn)]
-    {:ok, spawn_pid} = Task.Supervisor.start_child(pid, Livebook.Proxy.Handler, :serve, args)
-    monitor_ref = Process.monitor(spawn_pid)
+  @doc """
+  Handles a request by delegating to a new handler process in the
+  runtime.
+
+  This function blocks until the request handler is done and it returns
+  the final `conn`.
+  """
+  @spec serve(pid(), Plug.Conn.t()) :: Plug.Conn.t()
+  def serve(supervisor_pid, %Plug.Conn{} = conn) when is_pid(supervisor_pid) do
+    args = [self(), build_handler_conn(conn)]
+
+    {:ok, handler_pid} =
+      Task.Supervisor.start_child(supervisor_pid, Livebook.Proxy.Handler, :serve, args)
+
+    monitor_ref = Process.monitor(handler_pid)
     loop(monitor_ref, conn)
   end
 
-  defp build_client_conn(conn) do
+  defp build_handler_conn(conn) do
     %{
       adapter: nil,
       host: conn.host,
@@ -71,8 +95,8 @@ defmodule Livebook.Proxy.Server do
         send(pid, {ref, :ok})
         loop(monitor_ref, conn)
 
-      {:DOWN, ^monitor_ref, :process, _pid, reason} ->
-        {conn, reason}
+      {:DOWN, ^monitor_ref, :process, _pid, _reason} ->
+        conn
     end
   end
 end
diff --git a/lib/livebook/runtime.ex b/lib/livebook/runtime.ex
index c5430ce3f..4103b9aab 100644
--- a/lib/livebook/runtime.ex
+++ b/lib/livebook/runtime.ex
@@ -763,6 +763,8 @@ defprotocol Livebook.Runtime do
           source: atom()
         }
 
+  @type proxy_handler_spec :: {module :: module(), function :: atom(), args :: list()}
+
   @doc """
   Returns relevant information about the runtime.
 
@@ -1103,10 +1105,15 @@ defprotocol Livebook.Runtime do
   def unregister_clients(runtime, client_ids)
 
   @doc """
-  Fetches the running Proxy Handler's pid from runtime.
+  Fetches information about a proxy request handler, if available.
 
-  TODO: document the communication here.
+  When the handler is available, this function returns MFA. In order
+  to handle a connection, the caller should invoke the MFA, appending
+  `conn` to the argument list, where `conn` is a `%Plug.Conn{}` struct
+  for the specific request.
+
+  Once done, the handler MFA should return the final `conn`.
   """
-  @spec fetch_proxy_handler(t(), pid()) :: {:ok, pid()} | {:error, :not_found}
-  def fetch_proxy_handler(runtime, client_pid)
+  @spec fetch_proxy_handler_spec(t()) :: {:ok, proxy_handler_spec()} | {:error, :not_found}
+  def fetch_proxy_handler_spec(runtime)
 end
diff --git a/lib/livebook/runtime/attached.ex b/lib/livebook/runtime/attached.ex
index c6b409a56..8e79a4d6a 100644
--- a/lib/livebook/runtime/attached.ex
+++ b/lib/livebook/runtime/attached.ex
@@ -205,7 +205,7 @@ defimpl Livebook.Runtime, for: Livebook.Runtime.Attached do
     RuntimeServer.unregister_clients(runtime.server_pid, client_ids)
   end
 
-  def fetch_proxy_handler(runtime, client_pid) do
-    RuntimeServer.fetch_proxy_handler(runtime.server_pid, client_pid)
+  def fetch_proxy_handler_spec(runtime) do
+    RuntimeServer.fetch_proxy_handler_spec(runtime.server_pid)
   end
 end
diff --git a/lib/livebook/runtime/elixir_standalone.ex b/lib/livebook/runtime/elixir_standalone.ex
index 211d7904e..57d93ec13 100644
--- a/lib/livebook/runtime/elixir_standalone.ex
+++ b/lib/livebook/runtime/elixir_standalone.ex
@@ -324,7 +324,7 @@ defimpl Livebook.Runtime, for: Livebook.Runtime.ElixirStandalone do
     RuntimeServer.unregister_clients(runtime.server_pid, client_ids)
   end
 
-  def fetch_proxy_handler(runtime, client_pid) do
-    RuntimeServer.fetch_proxy_handler(runtime.server_pid, client_pid)
+  def fetch_proxy_handler_spec(runtime) do
+    RuntimeServer.fetch_proxy_handler_spec(runtime.server_pid)
   end
 end
diff --git a/lib/livebook/runtime/embedded.ex b/lib/livebook/runtime/embedded.ex
index 75b5e8ac7..c255cb076 100644
--- a/lib/livebook/runtime/embedded.ex
+++ b/lib/livebook/runtime/embedded.ex
@@ -171,8 +171,8 @@ defimpl Livebook.Runtime, for: Livebook.Runtime.Embedded do
     RuntimeServer.unregister_clients(runtime.server_pid, client_ids)
   end
 
-  def fetch_proxy_handler(runtime, client_pid) do
-    RuntimeServer.fetch_proxy_handler(runtime.server_pid, client_pid)
+  def fetch_proxy_handler_spec(runtime) do
+    RuntimeServer.fetch_proxy_handler_spec(runtime.server_pid)
   end
 
   defp config() do
diff --git a/lib/livebook/runtime/erl_dist/runtime_server.ex b/lib/livebook/runtime/erl_dist/runtime_server.ex
index 13f58a2d9..af8de4209 100644
--- a/lib/livebook/runtime/erl_dist/runtime_server.ex
+++ b/lib/livebook/runtime/erl_dist/runtime_server.ex
@@ -318,11 +318,14 @@ defmodule Livebook.Runtime.ErlDist.RuntimeServer do
   end
 
   @doc """
-  Fetches the running Proxy Handler's pid from runtime.
+  Fetches information about a proxy request handler, if available.
   """
-  @spec fetch_proxy_handler(pid(), pid()) :: {:ok, pid()} | {:error, :not_found}
-  def fetch_proxy_handler(pid, client_pid) do
-    GenServer.call(pid, {:fetch_proxy_handler, client_pid})
+  @spec fetch_proxy_handler_spec(pid()) ::
+          {:ok, {module(), atom(), list()}} | {:error, :not_found}
+  def fetch_proxy_handler_spec(pid) do
+    with {:ok, supervisor_pid} <- GenServer.call(pid, :fetch_proxy_handler_supervisor) do
+      {:ok, {Livebook.Proxy.Server, :serve, [supervisor_pid]}}
+    end
   end
 
   @doc """
@@ -752,9 +755,9 @@ defmodule Livebook.Runtime.ErlDist.RuntimeServer do
     {:reply, has_dependencies?, state}
   end
 
-  def handle_call({:fetch_proxy_handler, client_pid}, _from, state) do
-    if pid = Livebook.Proxy.Handler.get_pid(Kino.Proxy, client_pid) do
-      {:reply, {:ok, pid}, state}
+  def handle_call(:fetch_proxy_handler_supervisor, _from, state) do
+    if supervisor_pid = Livebook.Proxy.Handler.get_supervisor_pid() do
+      {:reply, {:ok, supervisor_pid}, state}
     else
       {:reply, {:error, :not_found}, state}
     end
diff --git a/lib/livebook/runtime/evaluator/io_proxy.ex b/lib/livebook/runtime/evaluator/io_proxy.ex
index 0c3c667da..ea06cf13a 100644
--- a/lib/livebook/runtime/evaluator/io_proxy.ex
+++ b/lib/livebook/runtime/evaluator/io_proxy.ex
@@ -383,7 +383,7 @@ defmodule Livebook.Runtime.Evaluator.IOProxy do
   end
 
   defp io_request({:livebook_get_proxy_handler_child_spec, fun}, state) do
-    result = {Livebook.Proxy.Handler, name: Kino.Proxy, listen: fun}
+    result = {Livebook.Proxy.Handler, listen: fun}
     {result, state}
   end
 
diff --git a/lib/livebook/session.ex b/lib/livebook/session.ex
index 20e9e008d..fdb839592 100644
--- a/lib/livebook/session.ex
+++ b/lib/livebook/session.ex
@@ -625,11 +625,12 @@ defmodule Livebook.Session do
   end
 
   @doc """
-  Fetches the running Proxy Handler's pid from runtime.
+  Fetches information about a proxy request handler, if available.
   """
-  @spec fetch_proxy_handler(pid(), pid()) :: {:ok, pid()} | {:error, :not_found | :disconnected}
-  def fetch_proxy_handler(pid, client_pid) do
-    GenServer.call(pid, {:fetch_proxy_handler, client_pid})
+  @spec fetch_proxy_handler_spec(pid()) ::
+          {:ok, Runtime.proxy_handler_spec()} | {:error, :not_found | :disconnected}
+  def fetch_proxy_handler_spec(pid) do
+    GenServer.call(pid, :fetch_proxy_handler_spec)
   end
 
   @doc """
@@ -1081,9 +1082,9 @@ defmodule Livebook.Session do
     {:noreply, state}
   end
 
-  def handle_call({:fetch_proxy_handler, client_pid}, _from, state) do
+  def handle_call(:fetch_proxy_handler_spec, _from, state) do
     if Runtime.connected?(state.data.runtime) do
-      {:reply, Runtime.fetch_proxy_handler(state.data.runtime, client_pid), state}
+      {:reply, Runtime.fetch_proxy_handler_spec(state.data.runtime), state}
     else
       {:reply, {:error, :disconnected}, state}
     end
diff --git a/lib/livebook_web/plugs/proxy_plug.ex b/lib/livebook_web/plugs/proxy_plug.ex
index 152830ace..5f1d266c0 100644
--- a/lib/livebook_web/plugs/proxy_plug.ex
+++ b/lib/livebook_web/plugs/proxy_plug.ex
@@ -1,5 +1,6 @@
 defmodule LivebookWeb.ProxyPlug do
   @behaviour Plug
+
   import Plug.Conn
 
   alias LivebookWeb.NotFoundError
@@ -10,10 +11,9 @@ defmodule LivebookWeb.ProxyPlug do
   @impl true
   def call(%{path_info: ["sessions", id, "proxy" | path_info]} = conn, _opts) do
     session = fetch_session!(id)
-    pid = fetch_proxy_handler!(session)
+    proxy_handler_spec = fetch_proxy_handler_spec!(session)
     conn = prepare_conn(conn, path_info, ["sessions", id, "proxy"])
-    {conn, _} = Livebook.Proxy.Server.serve(pid, Kino.Proxy, conn)
-
+    conn = call_proxy_handler(proxy_handler_spec, conn)
     halt(conn)
   end
 
@@ -25,10 +25,9 @@ defmodule LivebookWeb.ProxyPlug do
     end
 
     session = fetch_session!(id)
-    pid = fetch_proxy_handler!(session)
+    proxy_handler_spec = fetch_proxy_handler_spec!(session)
     conn = prepare_conn(conn, path_info, ["apps", slug, "proxy"])
-    {conn, _} = Livebook.Proxy.Server.serve(pid, Kino.Proxy, conn)
-
+    conn = call_proxy_handler(proxy_handler_spec, conn)
     halt(conn)
   end
 
@@ -50,8 +49,8 @@ defmodule LivebookWeb.ProxyPlug do
     end
   end
 
-  defp fetch_proxy_handler!(session) do
-    case Livebook.Session.fetch_proxy_handler(session.pid, self()) do
+  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"
     end
@@ -60,4 +59,9 @@ defmodule LivebookWeb.ProxyPlug do
   defp prepare_conn(conn, path_info, script_name) do
     %{conn | path_info: path_info, script_name: conn.script_name ++ script_name}
   end
+
+  defp call_proxy_handler(proxy_handler_spec, conn) do
+    {module, function, args} = proxy_handler_spec
+    apply(module, function, args ++ [conn])
+  end
 end
diff --git a/test/support/noop_runtime.ex b/test/support/noop_runtime.ex
index 4f3de233a..1c768ecde 100644
--- a/test/support/noop_runtime.ex
+++ b/test/support/noop_runtime.ex
@@ -73,7 +73,7 @@ defmodule Livebook.Runtime.NoopRuntime do
 
     def register_clients(_, _), do: :ok
     def unregister_clients(_, _), do: :ok
-    def fetch_proxy_handler(_, _), do: {:error, :not_found}
+    def fetch_proxy_handler_spec(_), do: {:error, :not_found}
 
     defp trace(runtime, fun, args) do
       if runtime.trace_to do