diff --git a/integrations/tests/tests/pointer-interactions.spec.tsx b/integrations/tests/tests/pointer-interactions.spec.tsx
index 73bc55e4a..5c904de50 100644
--- a/integrations/tests/tests/pointer-interactions.spec.tsx
+++ b/integrations/tests/tests/pointer-interactions.spec.tsx
@@ -405,6 +405,46 @@ test.describe("pointer interactions", () => {
   });
 
   test.describe("focus", () => {
+    for (const returnToStart of [false, true]) {
+      test(`should blur after dragging${returnToStart ? " back to the starting point" : ""}`, async ({
+        page: mainPage
+      }) => {
+        const page = await goToUrl(
+          mainPage,
+          <Group>
+            <Panel id="left" />
+            <Separator />
+            <Panel id="right" />
+          </Group>
+        );
+        const separator = page.getByRole("separator");
+        const { x, y } = getCenterCoordinates((await separator.boundingBox())!);
+
+        await page.mouse.move(x, y);
+        await page.mouse.down();
+        await expect(separator).toBeFocused();
+        await page.mouse.move(x + 25, y);
+        if (returnToStart) {
+          await page.mouse.move(x, y);
+        }
+        await page.mouse.up();
+        await expect(separator).not.toBeFocused();
+        const valueAfterDrag = await separator.getAttribute("aria-valuenow");
+        await page.keyboard.press("ArrowRight");
+        await expect(separator).toHaveAttribute(
+          "aria-valuenow",
+          valueAfterDrag!
+        );
+
+        // A subsequent click should still retain focus and support keyboard resizing.
+        await separator.click();
+        await expect(separator).toBeFocused();
+        const value = await separator.getAttribute("aria-valuenow");
+        await page.keyboard.press("ArrowRight");
+        await expect(separator).not.toHaveAttribute("aria-valuenow", value!);
+      });
+    }
+
     test("should update focus to the nearest separator", async ({
       page: mainPage
     }) => {
@@ -563,7 +603,8 @@ test.describe("pointer interactions", () => {
     await expect(separator).toHaveAttribute("data-separator", "active");
 
     await page.mouse.up();
-    await expect(separator).toHaveAttribute("data-separator", "focus");
+    await expect(separator).not.toBeFocused();
+    await expect(separator).not.toHaveAttribute("data-separator", "active");
 
     await page.mouse.move(0, 0);
     await page.mouse.down();
diff --git a/lib/components/group/ResizePreview.test.tsx b/lib/components/group/ResizePreview.test.tsx
index cd5daa3b6..3928ec2fa 100644
--- a/lib/components/group/ResizePreview.test.tsx
+++ b/lib/components/group/ResizePreview.test.tsx
@@ -205,6 +205,7 @@ describe("separator previews", () => {
     let interaction: InteractionActive = {
       state: "active",
       cursorFlags: 0,
+      didPointerMove: false,
       hitRegions: [],
       initialLayoutMap: new Map(),
       previewLayoutMap: new Map(),
diff --git a/lib/global/event-handlers/onDocumentPointerDown.ts b/lib/global/event-handlers/onDocumentPointerDown.ts
index b25344baa..c68f73e98 100644
--- a/lib/global/event-handlers/onDocumentPointerDown.ts
+++ b/lib/global/event-handlers/onDocumentPointerDown.ts
@@ -53,6 +53,7 @@ export function onDocumentPointerDown(event: PointerEvent) {
 
   updateInteractionState({
     cursorFlags: 0,
+    didPointerMove: false,
     hitRegions,
     initialLayoutMap,
     pointerDownAtPoint: { x: event.clientX, y: event.clientY },
diff --git a/lib/global/mutable-state/interactions.test.ts b/lib/global/mutable-state/interactions.test.ts
index b39191d9a..27dff8d64 100644
--- a/lib/global/mutable-state/interactions.test.ts
+++ b/lib/global/mutable-state/interactions.test.ts
@@ -35,6 +35,7 @@ test("removing a group preserves the other group in a shared drag", () => {
 
   updateInteractionState({
     cursorFlags: 0,
+    didPointerMove: false,
     hitRegions,
     initialLayoutMap,
     pointerDownAtPoint: { x: 100, y: 100 },
diff --git a/lib/global/mutable-state/interactions.ts b/lib/global/mutable-state/interactions.ts
index 66c013252..cb3826166 100644
--- a/lib/global/mutable-state/interactions.ts
+++ b/lib/global/mutable-state/interactions.ts
@@ -34,13 +34,15 @@ export function subscribeToInteractionState(
 export function updateCursorFlags(
   cursorFlags: number,
   previews: ResizePreview[] = [],
-  previewLayoutMap?: InteractionActive["previewLayoutMap"]
+  previewLayoutMap?: InteractionActive["previewLayoutMap"],
+  didPointerMove = false
 ) {
   const prev = state;
 
   const next = { ...state };
   next.cursorFlags = cursorFlags;
   if (next.state === "active") {
+    next.didPointerMove ||= didPointerMove;
     next.previews = previews;
     if (previewLayoutMap) {
       next.previewLayoutMap = previewLayoutMap;
@@ -60,6 +62,23 @@ export function updateInteractionState(next: InteractionState) {
 
   state = next;
 
+  // Keep click-to-focus behavior, but release keyboard focus after a drag.
+  // This also handles interactions completed by the missed-pointerup fallback.
+  if (
+    prev.state === "active" &&
+    next.state !== "active" &&
+    prev.didPointerMove
+  ) {
+    prev.hitRegions.forEach(({ separator }) => {
+      if (
+        separator &&
+        separator.element.ownerDocument.activeElement === separator.element
+      ) {
+        separator.element.blur();
+      }
+    });
+  }
+
   eventEmitter.emit("change", {
     prev,
     next
diff --git a/lib/global/mutable-state/types.ts b/lib/global/mutable-state/types.ts
index d695f7f15..545097822 100644
--- a/lib/global/mutable-state/types.ts
+++ b/lib/global/mutable-state/types.ts
@@ -27,6 +27,7 @@ export type ResizePreview = {
 
 export type InteractionActive = {
   cursorFlags: number;
+  didPointerMove: boolean;
   hitRegions: HitRegion[];
   initialLayoutMap: Map<RegisteredGroup, Layout>;
   pointerDownAtPoint: Point;
diff --git a/lib/global/utils/updateActiveHitRegion.test.ts b/lib/global/utils/updateActiveHitRegion.test.ts
index 1ea6aafa7..f99f6405d 100644
--- a/lib/global/utils/updateActiveHitRegion.test.ts
+++ b/lib/global/utils/updateActiveHitRegion.test.ts
@@ -48,6 +48,7 @@ describe("updateActiveHitRegions preview bounds", () => {
 
     updateInteractionState({
       cursorFlags: 0,
+      didPointerMove: false,
       hitRegions,
       initialLayoutMap,
       pointerDownAtPoint,
@@ -121,6 +122,7 @@ describe("updateActiveHitRegions preview bounds", () => {
           updateInteractionState({
             state: "active",
             cursorFlags: 0,
+            didPointerMove: false,
             hitRegions,
             initialLayoutMap,
             pointerDownAtPoint,
diff --git a/lib/global/utils/updateActiveHitRegion.ts b/lib/global/utils/updateActiveHitRegion.ts
index 69df15d87..8dd01ac4a 100644
--- a/lib/global/utils/updateActiveHitRegion.ts
+++ b/lib/global/utils/updateActiveHitRegion.ts
@@ -182,6 +182,11 @@ export function updateActiveHitRegions({
     cursorFlags |= nextCursorFlags & CURSOR_FLAGS_VERTICAL;
   }
 
-  updateCursorFlags(cursorFlags, previews, previewLayoutMap);
+  const didPointerMove =
+    interaction.state === "active" &&
+    (event.clientX !== interaction.pointerDownAtPoint.x ||
+      event.clientY !== interaction.pointerDownAtPoint.y);
+
+  updateCursorFlags(cursorFlags, previews, previewLayoutMap, didPointerMove);
   updateCursorStyle(document);
 }