diff --git a/desktop/src/app/routes/ChannelRouteScreen.tsx b/desktop/src/app/routes/ChannelRouteScreen.tsx
index 2855e44af..1e1b3ff43 100644
--- a/desktop/src/app/routes/ChannelRouteScreen.tsx
+++ b/desktop/src/app/routes/ChannelRouteScreen.tsx
@@ -168,6 +168,24 @@ export function ChannelRouteScreen({
   const effectiveAgentConversationReplyId = isChannelTasksEnabled
     ? targetAgentConversationReplyId
     : null;
+  const targetAgentConversationBackfillKey =
+    effectiveAgentConversationReplyId && !selectedPostId
+      ? [
+          channelId,
+          effectiveAgentConversationReplyId,
+          targetMessageId ?? "",
+          targetThreadRootId ?? "",
+        ].join(":")
+      : null;
+  const [
+    completedTargetAgentConversationBackfillKey,
+    setCompletedTargetAgentConversationBackfillKey,
+  ] = React.useState<string | null>(null);
+  const targetAgentConversationBackfillPending = Boolean(
+    targetAgentConversationBackfillKey &&
+      completedTargetAgentConversationBackfillKey !==
+        targetAgentConversationBackfillKey,
+  );
 
   // Reset spliced target events when the channel context changes (channel
   // switch or entering/leaving a forum post). Tied to channel identity rather
@@ -201,6 +219,7 @@ export function ChannelRouteScreen({
         !targetThreadRootId) ||
       selectedPostId
     ) {
+      setCompletedTargetAgentConversationBackfillKey(null);
       return () => {
         isCancelled = true;
       };
@@ -233,21 +252,29 @@ export function ChannelRouteScreen({
       effectiveAgentConversationReplyId ?? targetMessageId,
       effectiveAgentConversationReplyId,
       targetThreadRootId,
-    ).then((events) => {
-      if (!isCancelled) {
-        queryClient.setQueryData<RelayEvent[]>(
-          channelMessagesKey(channelId),
-          (currentEvents) => mergeRouteEvents(currentEvents, events),
-        );
-        setTargetMessageEvents((currentEvents) => {
-          const eventsById = new Map<string, RelayEvent>();
-          for (const event of [...currentEvents, ...events]) {
-            eventsById.set(event.id, event);
-          }
-          return Array.from(eventsById.values());
-        });
-      }
-    });
+    )
+      .then((events) => {
+        if (!isCancelled) {
+          queryClient.setQueryData<RelayEvent[]>(
+            channelMessagesKey(channelId),
+            (currentEvents) => mergeRouteEvents(currentEvents, events),
+          );
+          setTargetMessageEvents((currentEvents) => {
+            const eventsById = new Map<string, RelayEvent>();
+            for (const event of [...currentEvents, ...events]) {
+              eventsById.set(event.id, event);
+            }
+            return Array.from(eventsById.values());
+          });
+        }
+      })
+      .finally(() => {
+        if (!isCancelled && targetAgentConversationBackfillKey) {
+          setCompletedTargetAgentConversationBackfillKey(
+            targetAgentConversationBackfillKey,
+          );
+        }
+      });
 
     return () => {
       isCancelled = true;
@@ -257,6 +284,7 @@ export function ChannelRouteScreen({
     channelId,
     queryClient,
     effectiveAgentConversationReplyId,
+    targetAgentConversationBackfillKey,
     targetMessageId,
     targetThreadRootId,
   ]);
@@ -283,6 +311,9 @@ export function ChannelRouteScreen({
       }}
       selectedForumPostId={selectedPostId}
       targetAgentConversationReplyId={effectiveAgentConversationReplyId}
+      targetAgentConversationBackfillPending={
+        targetAgentConversationBackfillPending
+      }
       targetForumReplyId={targetReplyId}
       targetMessageEvents={targetMessageEvents}
       targetMessageId={targetMessageId}
diff --git a/desktop/src/features/channels/ui/ChannelScreen.tsx b/desktop/src/features/channels/ui/ChannelScreen.tsx
index 3d7ddc6af..ac79b84d4 100644
--- a/desktop/src/features/channels/ui/ChannelScreen.tsx
+++ b/desktop/src/features/channels/ui/ChannelScreen.tsx
@@ -88,6 +88,7 @@ export function ChannelScreen({
   onCloseForumPost,
   onSelectForumPost,
   selectedForumPostId,
+  targetAgentConversationBackfillPending = false,
   targetAgentConversationReplyId,
   targetForumReplyId,
   targetMessageEvents,
@@ -743,6 +744,7 @@ export function ChannelScreen({
     goChannel,
     messageProfilesReady,
     openAgentConversation,
+    targetBackfillPending: targetAgentConversationBackfillPending,
     targetAgentConversationReplyId: isChannelTasksEnabled
       ? targetAgentConversationReplyId
       : null,
diff --git a/desktop/src/features/channels/ui/ChannelScreen.types.ts b/desktop/src/features/channels/ui/ChannelScreen.types.ts
index 5401c44b1..24c23745a 100644
--- a/desktop/src/features/channels/ui/ChannelScreen.types.ts
+++ b/desktop/src/features/channels/ui/ChannelScreen.types.ts
@@ -12,6 +12,7 @@ export type ChannelScreenProps = {
   onCloseForumPost: () => void;
   onSelectForumPost: (postId: string) => void;
   selectedForumPostId: string | null;
+  targetAgentConversationBackfillPending?: boolean;
   targetAgentConversationReplyId: string | null;
   targetForumReplyId: string | null;
   targetMessageEvents: RelayEvent[];
diff --git a/desktop/src/features/channels/ui/useAgentConversationRouteTarget.ts b/desktop/src/features/channels/ui/useAgentConversationRouteTarget.ts
index b4e7029d6..09f10bbd2 100644
--- a/desktop/src/features/channels/ui/useAgentConversationRouteTarget.ts
+++ b/desktop/src/features/channels/ui/useAgentConversationRouteTarget.ts
@@ -31,6 +31,7 @@ type UseAgentConversationRouteTargetInput = {
     input: OpenAgentConversationInput,
     options?: { publishMarker?: boolean },
   ) => void;
+  targetBackfillPending: boolean;
   targetAgentConversationReplyId: string | null;
   timelineMessages: readonly TimelineMessage[];
 };
@@ -63,6 +64,7 @@ export function useAgentConversationRouteTarget({
   goChannel,
   messageProfilesReady,
   openAgentConversation,
+  targetBackfillPending,
   targetAgentConversationReplyId,
   timelineMessages,
 }: UseAgentConversationRouteTargetInput) {
@@ -98,6 +100,9 @@ export function useAgentConversationRouteTarget({
     if (!sourceMessage) {
       return;
     }
+    if (!marker && targetBackfillPending) {
+      return;
+    }
     if (!marker?.agentPubkey && !agentLookupReady) {
       return;
     }
@@ -160,6 +165,7 @@ export function useAgentConversationRouteTarget({
     goChannel,
     messageProfilesReady,
     openAgentConversation,
+    targetBackfillPending,
     targetAgentConversationReplyId,
     timelineMessages,
   ]);