diff --git a/CHANGELOG.md b/CHANGELOG.md
index 87e0d54435..e6d2e04068 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -2,6 +2,8 @@
 
 ## Bug fixes
 
+  * [Phoenix.Transports.LongPoll] Keep a publish when its listen has already
+    expired, and return that publish on the next listen
   * [Phoenix.ChannelTest] Fix test sockets violating the Phoenix.Socket.t
     typespec, which made Dialyzer treat every test join as never returning
     ([#5509](https://github.com/phoenixframework/phoenix/issues/5509))
diff --git a/lib/phoenix/transports/long_poll.ex b/lib/phoenix/transports/long_poll.ex
index 4085e1abf7..824c0b83ae 100644
--- a/lib/phoenix/transports/long_poll.ex
+++ b/lib/phoenix/transports/long_poll.ex
@@ -175,13 +175,11 @@ defmodule Phoenix.Transports.LongPoll do
             {:messages, messages, ^ref} -> {:ok, messages}
           after
             opts[:window_ms] ->
-              broadcast_from!(endpoint, server_ref, {:expired, client_ref, ref})
-              {:no_content, []}
+              expire_listen(endpoint, server_ref, client_ref, ref)
           end
       after
         opts[:window_ms] ->
-          broadcast_from!(endpoint, server_ref, {:expired, client_ref, ref})
-          {:no_content, []}
+          expire_listen(endpoint, server_ref, client_ref, ref)
       end
 
     conn
@@ -189,6 +187,19 @@ defmodule Phoenix.Transports.LongPoll do
     |> status_token_messages_json(token, messages)
   end
 
+  # A publish can arrive in the same moment the timer fires. Take it when it
+  # is already in this mailbox. The session keeps its buffer when this expired
+  # notice is already queued there.
+  defp expire_listen(endpoint, server_ref, client_ref, ref) do
+    broadcast_from!(endpoint, server_ref, {:expired, client_ref, ref})
+
+    receive do
+      {:messages, messages, ^ref} -> {:ok, messages}
+    after
+      0 -> {:no_content, []}
+    end
+  end
+
   # Accept the token from either location so that newer clients can use the
   # header while older clients continue to use params.
   defp fetch_token(conn) do
diff --git a/lib/phoenix/transports/long_poll_server.ex b/lib/phoenix/transports/long_poll_server.ex
index e3a5f23d8d..41af5fbde6 100644
--- a/lib/phoenix/transports/long_poll_server.ex
+++ b/lib/phoenix/transports/long_poll_server.ex
@@ -73,12 +73,21 @@ defmodule Phoenix.Transports.LongPoll.Server do
   end
 
   def handle_info({:flush, client_ref, ref}, state) do
-    case state.buffer do
-      [] ->
+    cond do
+      # This listen already gave up. A send now would miss it and drop the buffer.
+      expired_queued?(client_ref, ref) ->
+        {:noreply,
+         %{
+           state
+           | client_ref: clear_client(state.client_ref, client_ref, ref),
+             last_client_poll: now_ms()
+         }}
+
+      state.buffer == [] ->
         {:noreply, %{state | client_ref: {client_ref, ref}, last_client_poll: now_ms()}}
 
-      buffer ->
-        broadcast_from!(state, client_ref, {:messages, Enum.reverse(buffer), ref})
+      true ->
+        broadcast_from!(state, client_ref, {:messages, Enum.reverse(state.buffer), ref})
         {:noreply, %{state | client_ref: nil, last_client_poll: now_ms(), buffer: []}}
     end
   end
@@ -153,6 +162,14 @@ defmodule Phoenix.Transports.LongPoll.Server do
     end
   end
 
+  defp expired_queued?(client_ref, ref) do
+    {:messages, mailbox} = Process.info(self(), :messages)
+    Enum.any?(mailbox, &match?({:expired, ^client_ref, ^ref}, &1))
+  end
+
+  defp clear_client({client_ref, ref}, client_ref, ref), do: nil
+  defp clear_client(client_ref, _client_ref, _ref), do: client_ref
+
   defp now_ms, do: System.system_time(:millisecond)
 
   defp schedule_inactive_shutdown(window_ms) do
diff --git a/test/phoenix/integration/long_poll_channels_test.exs b/test/phoenix/integration/long_poll_channels_test.exs
index 2513f61b66..65574618e1 100644
--- a/test/phoenix/integration/long_poll_channels_test.exs
+++ b/test/phoenix/integration/long_poll_channels_test.exs
@@ -281,6 +281,74 @@ defmodule Phoenix.Integration.LongPollChannelsTest do
 
   defp encode(V1.JSONSerializer, %{} = map), do: Phoenix.json_library().encode!(map)
 
+  # Queues a join behind the heartbeat, then holds the session before that
+  # join runs. The listen's later flush is already behind the join.
+  defp hold_expired_join(state, body, opcode, client, parent, release) do
+    cond do
+      String.contains?(body, "\"heartbeat\"") ->
+        join = ~s(["join-1","join-1","room:lobby","phx_join",{}])
+        send(self(), {:dispatch, client, {join, opcode}, make_ref()})
+        state
+
+      String.contains?(body, "\"phx_join\"") ->
+        send(parent, :join_blocked)
+
+        receive do
+          {^release, :release} -> state
+        end
+
+      true ->
+        state
+    end
+  end
+
+  defp await_parked_listen(pid) do
+    Enum.reduce_while(1..100, :waiting, fn _, _ ->
+      case :sys.get_state(pid) do
+        %{client_ref: {listen_pid, _ref}} when is_pid(listen_pid) ->
+          {:halt, listen_pid}
+
+        _ ->
+          Process.sleep(2)
+          {:cont, :waiting}
+      end
+    end)
+    |> case do
+      listen_pid when is_pid(listen_pid) -> listen_pid
+      :waiting -> flunk("long-poll listen did not park")
+    end
+  end
+
+  defp await_expired_flush(server) do
+    Enum.reduce_while(1..100, :waiting, fn _, _ ->
+      case Process.info(server, :messages) do
+        {:messages, mailbox} ->
+          flush? = Enum.any?(mailbox, &match?({:flush, _, _}, &1))
+          expired? = Enum.any?(mailbox, &match?({:expired, _, _}, &1))
+
+          if flush? and expired? do
+            {:halt, :ok}
+          else
+            Process.sleep(20)
+            {:cont, :waiting}
+          end
+
+        nil ->
+          flunk("long-poll session ended before the expired flush was queued")
+      end
+    end)
+    |> case do
+      :ok -> :ok
+      :waiting -> flunk("second flush and expired notice were not both queued")
+    end
+  end
+
+  defp resume_if_suspended(pid) do
+    if Process.alive?(pid) and match?({:status, :suspended}, Process.info(pid, :status)) do
+      :erlang.resume_process(pid)
+    end
+  end
+
   @doc """
   Joins a long poll socket.
 
@@ -788,6 +856,78 @@ defmodule Phoenix.Integration.LongPollChannelsTest do
         assert resp.body["status"] == 408
       end
 
+      test "a reply published while a listen has expired is on the next listen" do
+        resp = poll(:get, "/ws", "2.0.0", %{}, nil)
+        assert resp.body["status"] == 410
+        assert resp.status == 200
+        token = resp.body["token"]
+        session = %{"token" => token}
+
+        {:ok, {:v1, _id, server, _topic}} =
+          Phoenix.Token.verify(Endpoint, Atom.to_string(__MODULE__), token)
+
+        release = make_ref()
+        parent = self()
+
+        :ok =
+          :sys.install(
+            server,
+            {fn state, event, _name ->
+               case event do
+                 {:in, {:dispatch, client, {body, opcode}, _ref}} when is_binary(body) ->
+                   hold_expired_join(state, body, opcode, client, parent, release)
+
+                 _ ->
+                   state
+               end
+             end, nil}
+          )
+
+        on_exit(fn ->
+          if Process.alive?(server) do
+            send(server, {release, :release})
+            Process.exit(server, :kill)
+          end
+        end)
+
+        listen = Task.async(fn -> poll(:get, "/ws", "2.0.0", session) end)
+        listen_pid = await_parked_listen(server)
+        on_exit(fn -> resume_if_suspended(listen_pid) end)
+        :erlang.suspend_process(listen_pid)
+
+        poster =
+          Task.async(fn ->
+            poll(:post, "/ws", "2.0.0", session, %{
+              "topic" => "phoenix",
+              "event" => "heartbeat",
+              "ref" => "hb-1",
+              "payload" => %{}
+            })
+          end)
+
+        assert_receive :join_blocked, 1_000
+        :erlang.resume_process(listen_pid)
+        assert await_expired_flush(server)
+        send(server, {release, :release})
+
+        first = Task.await(listen, 5_000)
+        assert first.status == 200
+        assert first.body["status"] == 204
+        assert first.body["messages"] == []
+
+        post = Task.await(poster, 5_000)
+        assert post.status == 200
+        assert post.body["status"] == 200
+
+        next = poll(:get, "/ws", "2.0.0", session)
+        assert next.status == 200
+        assert next.body["status"] == 200
+
+        assert Enum.any?(next.body["messages"], fn message ->
+                 message.ref == "join-1" or message.join_ref == "join-1"
+               end)
+      end
+
       test "ignores ndjson batch entries after the first 100", %{topic: topic} do
         vsn = "2.0.0"
         join_ref = "1"