diff --git a/packages/app/e2e/agent-timeline-pagination.spec.ts b/packages/app/e2e/agent-timeline-pagination.spec.ts
index 31d381ed27..9b485caf3c 100644
--- a/packages/app/e2e/agent-timeline-pagination.spec.ts
+++ b/packages/app/e2e/agent-timeline-pagination.spec.ts
@@ -1,6 +1,7 @@
 import { expect, test } from "./fixtures";
 import {
   expectSameOlderHistoryLoadingOperation,
+  expectStableHistoryStartGutter,
   expectTimelineAtHistoryStart,
   expectTimelinePromptCentered,
   expectTimelinePromptNotMounted,
@@ -27,6 +28,27 @@ import {
 } from "./helpers/timeline-pagination";
 
 test.describe("Agent timeline pagination", () => {
+  test("keeps a fixed history-start gutter before, during, and after pagination", async ({
+    page,
+  }) => {
+    const agent = await seedLongMockAgentTimeline({ turns: 40 });
+    try {
+      const history = await holdOlderHistoryPages(page, agent);
+      await openAgentTimeline(page, agent);
+      await expectStableHistoryStartGutter(page);
+
+      await userScrollsTimelineToHistoryStart(page);
+      await history.expectRequestedPages(1);
+      await expectStableHistoryStartGutter(page);
+
+      history.releasePage(1);
+      await history.expectSettledWithRequestedPages(1);
+      await expectStableHistoryStartGutter(page);
+    } finally {
+      await agent.cleanup();
+    }
+  });
+
   test("loads one page each time the user returns to history start", async ({ page }) => {
     test.setTimeout(120_000);
     const agent = await seedLongMockAgentTimeline({ turns: 80 });
diff --git a/packages/app/e2e/helpers/timeline-pagination.ts b/packages/app/e2e/helpers/timeline-pagination.ts
index 2b00a980ba..866782521c 100644
--- a/packages/app/e2e/helpers/timeline-pagination.ts
+++ b/packages/app/e2e/helpers/timeline-pagination.ts
@@ -286,6 +286,14 @@ export async function rememberTimelineViewport(page: Page): Promise<TimelineView
   return readTimelineViewport(page);
 }
 
+export async function expectStableHistoryStartGutter(page: Page): Promise<void> {
+  const gutter = page.getByTestId("older-history-slot");
+  await expect(gutter).toBeAttached();
+  await expect
+    .poll(() => gutter.evaluate((element) => element.getBoundingClientRect().height))
+    .toBe(32);
+}
+
 export async function scrollTimelinePromptIntoView(page: Page, prompt: string): Promise<void> {
   const timeline = page.locator('[data-testid="agent-chat-scroll"]:visible').first();
   const row = timeline.getByTestId("user-message").filter({ hasText: prompt });
diff --git a/packages/app/src/agent-stream/history-start-pagination.test.ts b/packages/app/src/agent-stream/history-start-pagination.test.ts
index 3a23fd18b3..475dbc771c 100644
--- a/packages/app/src/agent-stream/history-start-pagination.test.ts
+++ b/packages/app/src/agent-stream/history-start-pagination.test.ts
@@ -4,7 +4,6 @@ import {
   createHistoryStartPaginationState,
   evaluateHistoryStartPagination,
   isHistoryStartLoadingOperation,
-  isHistoryStartSlotReserved,
   rearmHistoryStartPagination,
   settleHistoryStartPagination,
   type HistoryStartPaginationInput,
@@ -23,15 +22,11 @@ const visibleHistoryStart: HistoryStartPaginationInput = {
 };
 
 describe("history start pagination", () => {
-  it("waits for user scroll intent before loading or reserving the loader slot", () => {
+  it("waits for user scroll intent before loading", () => {
     const dormant = createHistoryStartPaginationState();
     const evaluated = evaluateHistoryStartPagination(dormant, visibleHistoryStart);
 
     expect(evaluated).toEqual({ state: { status: "dormant" }, shouldLoad: false });
-    expect(isHistoryStartSlotReserved(evaluated.state, true)).toBe(false);
-    expect(isHistoryStartSlotReserved(rearmHistoryStartPagination(evaluated.state), true)).toBe(
-      true,
-    );
   });
 
   it("waits for anchored page geometry before authorizing another page", () => {
diff --git a/packages/app/src/agent-stream/history-start-pagination.ts b/packages/app/src/agent-stream/history-start-pagination.ts
index 8edbbe475a..46914ae3e1 100644
--- a/packages/app/src/agent-stream/history-start-pagination.ts
+++ b/packages/app/src/agent-stream/history-start-pagination.ts
@@ -34,13 +34,6 @@ export function rearmHistoryStartPagination(
   return state.status === "dormant" || state.status === "latched" ? { status: "ready" } : state;
 }
 
-export function isHistoryStartSlotReserved(
-  state: HistoryStartPaginationState,
-  hasOlderHistory: boolean,
-): boolean {
-  return state.status !== "dormant" && (hasOlderHistory || state.status !== "ready");
-}
-
 export function abandonHistoryStartPaginationRequest(
   state: HistoryStartPaginationState,
   requestedProgressKey: string,
diff --git a/packages/app/src/agent-stream/strategy-native.tsx b/packages/app/src/agent-stream/strategy-native.tsx
index 1d0a7c17fa..788e4a38a7 100644
--- a/packages/app/src/agent-stream/strategy-native.tsx
+++ b/packages/app/src/agent-stream/strategy-native.tsx
@@ -36,7 +36,6 @@ import {
   createHistoryStartPaginationState,
   evaluateHistoryStartPagination,
   isHistoryStartLoadingOperation,
-  isHistoryStartSlotReserved,
   rearmHistoryStartPagination,
   settleHistoryStartPagination,
   type HistoryStartPaginationInput,
@@ -59,9 +58,8 @@ const foregroundMutedColorMapping = (theme: Theme) => ({
 const historyStartSlotStyle: ViewStyle = {
   alignItems: "center",
   justifyContent: "center",
-  minHeight: 32,
-  paddingTop: 4,
-  paddingBottom: 8,
+  height: 32,
+  flexShrink: 0,
 };
 const HISTORY_START_SETTLE_FRAMES = 2;
 
@@ -584,20 +582,16 @@ function NativeStreamViewport(props: StreamRenderInput & { strategy: StreamStrat
 
   const historyFooterContent = useMemo(() => {
     const isLoadingOperation = isHistoryStartLoadingOperation(historyStartPaginationState);
-    if (!isHistoryStartSlotReserved(historyStartPaginationState, hasOlderHistory)) {
-      return null;
-    }
     return (
-      <View
-        style={historyStartSlotStyle}
-        testID={isLoadingOperation ? "load-older-history-spinner" : undefined}
-      >
+      <View style={historyStartSlotStyle} testID="older-history-slot">
         {isLoadingOperation ? (
-          <ThemedLoadingSpinner size="small" uniProps={foregroundMutedColorMapping} />
+          <View testID="load-older-history-spinner">
+            <ThemedLoadingSpinner size="small" uniProps={foregroundMutedColorMapping} />
+          </View>
         ) : null}
       </View>
     );
-  }, [hasOlderHistory, historyStartPaginationState]);
+  }, [historyStartPaginationState]);
 
   // RN's FlatList strictMode keeps its internal renderItem wrapper stable when
   // data or the live header changes, preserving the row identities above.
diff --git a/packages/app/src/agent-stream/strategy-web.tsx b/packages/app/src/agent-stream/strategy-web.tsx
index 3cd6cf88fa..3a83007e23 100644
--- a/packages/app/src/agent-stream/strategy-web.tsx
+++ b/packages/app/src/agent-stream/strategy-web.tsx
@@ -21,7 +21,6 @@ import {
   createHistoryStartPaginationState,
   evaluateHistoryStartPagination,
   isHistoryStartLoadingOperation,
-  isHistoryStartSlotReserved,
   rearmHistoryStartPagination,
   settleHistoryStartPagination,
   type HistoryStartPaginationInput,
@@ -69,9 +68,8 @@ const historyStartSlotStyle: CSSProperties = {
   display: "flex",
   alignItems: "center",
   justifyContent: "center",
-  minHeight: 32,
-  paddingTop: 4,
-  paddingBottom: 8,
+  height: 32,
+  flexShrink: 0,
 };
 
 const mountedHistoryRowStyle: CSSProperties = {
@@ -785,20 +783,16 @@ function WebStreamViewport(props: StreamRenderInput & { isMobileBreakpoint: bool
   }, [renderLiveAuxiliary]);
   const historyStartSlot = useMemo(() => {
     const isLoadingOperation = isHistoryStartLoadingOperation(historyStartPaginationState);
-    if (!isHistoryStartSlotReserved(historyStartPaginationState, hasOlderHistory)) {
-      return null;
-    }
     return (
-      <div
-        style={historyStartSlotStyle}
-        data-testid={isLoadingOperation ? "load-older-history-spinner" : undefined}
-      >
+      <div style={historyStartSlotStyle} data-testid="older-history-slot">
         {isLoadingOperation ? (
-          <ThemedLoadingSpinner size="small" uniProps={foregroundMutedColorMapping} />
+          <div data-testid="load-older-history-spinner">
+            <ThemedLoadingSpinner size="small" uniProps={foregroundMutedColorMapping} />
+          </div>
         ) : null}
       </div>
     );
-  }, [hasOlderHistory, historyStartPaginationState]);
+  }, [historyStartPaginationState]);
   const shouldRenderEmpty =
     !boundary.hasMountedHistory &&
     !boundary.hasVirtualizedHistory &&