diff --git a/scripts/check-unread-tracker.ts b/scripts/check-unread-tracker.ts
index c49019180..df7e06f45 100644
--- a/scripts/check-unread-tracker.ts
+++ b/scripts/check-unread-tracker.ts
@@ -12,6 +12,7 @@ const {
   markChannelRead,
   markChannelUnread,
   markServerRead,
+  setServerUnread,
 } = await import("../src/packages/common/src/hooks/useUnreadTracker.ts");
 
 const counts = (host: string) => getUnreadSnapshot().get(host) ?? new Map();
@@ -65,4 +66,20 @@ assert.equal(total(HOST), 0);
 // And leaves the other server alone.
 assert.equal(total(OTHER), 1);
 
+// The server's counts replace this window's for each conversation it has a marker for,
+// and leave the rest alone.
+markServerRead(OTHER);
+markChannelUnread(HOST, "local-only");
+markChannelUnread(HOST, "marked");
+setServerUnread(HOST, { marked: 4 }, ["marked", "caught-up"]);
+assert.equal(counts(HOST).get("marked"), 4);
+assert.equal(counts(HOST).get("local-only"), 1);
+assert.equal(counts(HOST).get("caught-up"), undefined);
+
+// A marker with no count means caught up, and the last one leaves no empty map behind.
+markServerRead(HOST);
+markChannelUnread(HOST, "marked");
+setServerUnread(HOST, {}, ["marked"]);
+assert.equal(getUnreadSnapshot().has(HOST), false);
+
 console.log("unread tracker: ok");
diff --git a/src/packages/common/src/hooks/useUnreadTracker.ts b/src/packages/common/src/hooks/useUnreadTracker.ts
index 3d9551bee..927ef7537 100644
--- a/src/packages/common/src/hooks/useUnreadTracker.ts
+++ b/src/packages/common/src/hooks/useUnreadTracker.ts
@@ -1,8 +1,8 @@
 import { useCallback, useSyncExternalStore } from "react";
 
 /**
- * How many messages have arrived in a conversation that nobody has looked at.
- * **Counted from when this window connected**, not from a server-side marker.
+ * How many messages have arrived in a conversation that nobody has looked at. Seeded from
+ * the server's read markers when a connection opens, then counted here as more arrive.
  */
 type UnreadMap = Map<string, Map<string, number>>;
 
@@ -56,6 +56,25 @@ export function markChannelRead(host: string, channelId: string) {
   emitChange();
 }
 
+/**
+ * What the server says, for every conversation it holds a marker for. One with no marker
+ * keeps what this window counted, since the server has nothing to say about it.
+ */
+export function setServerUnread(host: string, counts: Record<string, number>, marked: Iterable<string>) {
+  const fresh = new Map(unreadMap.get(host));
+  for (const channelId of marked) fresh.delete(channelId);
+  for (const [channelId, n] of Object.entries(counts)) {
+    if (n > 0) fresh.set(channelId, n);
+  }
+
+  /* Dropped rather than left empty, so serverHasUnread stays a size check. */
+  const next = new Map(unreadMap);
+  if (fresh.size === 0) next.delete(host);
+  else next.set(host, fresh);
+  unreadMap = next;
+  emitChange();
+}
+
 export function markServerRead(host: string) {
   if (!unreadMap.has(host)) return;
   const next = new Map(unreadMap);
diff --git a/src/packages/socket/src/components/MarkAsReadItem.tsx b/src/packages/socket/src/components/MarkAsReadItem.tsx
index 877234fda..0a80ab65e 100644
--- a/src/packages/socket/src/components/MarkAsReadItem.tsx
+++ b/src/packages/socket/src/components/MarkAsReadItem.tsx
@@ -6,6 +6,7 @@ import {
   clearServerMentions,
   clearServerThreadMentions,
   clearServerThreadUnread,
+  getUnreadSnapshot,
   markChannelRead,
   markConversationThreadsRead,
   markServerRead,
@@ -57,10 +58,12 @@ export function MarkAsReadItem({ host, scope }: { host: string; scope: MarkReadS
     /* Threads and all, which opening the channel deliberately does not do
        (GRYT-1014). This is somebody saying they are finished with it. */
     sockets[host]?.emit("mentions:seen", { conversationId: id, includeThreads: true });
+    sockets[host]?.emit("read:set", { conversationId: id });
   };
 
   const onClick = () => {
     if (scope.kind === "server") {
+      for (const id of getUnreadSnapshot().get(host)?.keys() ?? []) sockets[host]?.emit("read:set", { conversationId: id });
       markServerRead(host);
       clearServerMentions(host);
       clearServerThreadUnread(host);
diff --git a/src/packages/socket/src/components/serverView.tsx b/src/packages/socket/src/components/serverView.tsx
index efb691637..4a7dd34e5 100644
--- a/src/packages/socket/src/components/serverView.tsx
+++ b/src/packages/socket/src/components/serverView.tsx
@@ -260,8 +260,11 @@ export const ServerView = ({ dmSpace = false }: { dmSpace?: boolean }) => {
   useEffect(() => {
     if (!currentlyViewingServer) return;
     const opened = visibleDmId || visibleChannelId;
-    if (opened) markChannelRead(currentlyViewingServer.host, opened);
-  }, [currentlyViewingServer, visibleChannelId, visibleDmId]);
+    if (!opened) return;
+    markChannelRead(currentlyViewingServer.host, opened);
+    // No message id: the server reads up to its newest. It ignores a DM.
+    sockets[currentlyViewingServer.host]?.emit("read:set", { conversationId: opened });
+  }, [currentlyViewingServer, visibleChannelId, visibleDmId, sockets]);
 
   useEffect(() => {
     setOnScreenConversation(currentlyViewingServer?.host ?? null, visibleDmId || visibleChannelId);
diff --git a/src/packages/socket/src/hooks/registerServerSocketEvents.ts b/src/packages/socket/src/hooks/registerServerSocketEvents.ts
index 9599435c6..6c91d8868 100644
--- a/src/packages/socket/src/hooks/registerServerSocketEvents.ts
+++ b/src/packages/socket/src/hooks/registerServerSocketEvents.ts
@@ -22,6 +22,7 @@ import {
   setServerFileAccess,
   setServerNotice,
   setServerRefreshToken,
+  setServerUnread,
   setThreadMentionCounts,
   subscribeToPrefs,
 } from "@/common";
@@ -215,6 +216,22 @@ export function registerServerSocketEvents(socket: Socket, host: string, ctx: Se
     socket.emit("mentions:list");
   }
 
+  /* Read markers, asked for on the same moments as mentions and for the same reason: a
+     reload, a reconnect and a rejoin are each a point the counts have gone stale. */
+  let askedForRead = false;
+  socket.on("disconnect", () => { askedForRead = false; });
+
+  function askForRead() {
+    askedForRead = true;
+    socket.emit("read:list");
+  }
+
+  /* One name for the question and the answer, as mentions does, so a second window
+     cannot end up disagreeing about what is left. */
+  socket.on("read:list", (payload: { counts?: Record<string, number>; markers?: { conversation_id: string }[] }) => {
+    setServerUnread(host, payload?.counts ?? {}, (payload?.markers ?? []).map((m) => m.conversation_id));
+  });
+
   const { nickname, userIdRef, servers, serversRef, lastInviteJoinAttemptRef, myVoiceStateByHostRef } = ctx;
   const { setServers, setNewServerInfo, setServerDetailsList, setFailedServerDetails } = ctx;
   const { setClients, setMemberLists, setMemberKeyStates, setServerProfiles, setIsServerMuted, setIsServerDeafened } = ctx;
@@ -347,6 +364,7 @@ export function registerServerSocketEvents(socket: Socket, host: string, ctx: Se
     /* A reload never gets `server:joined`, so this was the only event left that
        says the session is back and the member is known (GRYT-1388). */
     if (!askedForMentions) askForMentions();
+    if (!askedForRead) askForRead();
 
     // Not awaited: a key that never arrives means no encrypted messages rather
     // than a connection that failed.
@@ -436,6 +454,7 @@ export function registerServerSocketEvents(socket: Socket, host: string, ctx: Se
     // Every join, not just the first: being away is when this accumulates, and it
     // is how a mention read on a phone stops showing here.
     askForMentions();
+    askForRead();
 
     // Read when the event fires, not at registration: the socket exists before
     // `useUserId` resolves, so a captured value was usually null.
diff --git a/src/packages/socket/src/hooks/useChat.ts b/src/packages/socket/src/hooks/useChat.ts
index 0e0e3c7fd..434d6bf6e 100644
--- a/src/packages/socket/src/hooks/useChat.ts
+++ b/src/packages/socket/src/hooks/useChat.ts
@@ -494,6 +494,9 @@ export function useChat({
           warnUnreadOnScreen("useChat chat:new", { serverHost, activeConversationId });
         }
         markChannelUnread(serverHost, msg.conversation_id);
+      } else if (msg.conversation_id === activeConversationId && msg.sender_server_id !== currentUserId) {
+        // Read as it arrives, so the server's marker keeps up with the screen. The server ignores a DM.
+        currentConnection.emit("read:set", { conversationId: msg.conversation_id, messageId: msg.message_id });
       }
       /* The same question `useSocketEvents` asks for a background server, so the
          two cannot disagree about focus, a mention, the channel default or a mute. */