diff --git a/packages/react-resizable-panels/src/PanelResizeHandle.test.tsx b/packages/react-resizable-panels/src/PanelResizeHandle.test.tsx
index 60cf81852..256036921 100644
--- a/packages/react-resizable-panels/src/PanelResizeHandle.test.tsx
+++ b/packages/react-resizable-panels/src/PanelResizeHandle.test.tsx
@@ -3,7 +3,11 @@ import { act } from "react-dom/test-utils";
 import { Panel, PanelGroup, PanelResizeHandle } from ".";
 import { assert } from "./utils/assert";
 import { getResizeHandleElement } from "./utils/dom/getResizeHandleElement";
-import { dispatchPointerEvent } from "./utils/test-utils";
+import {
+  dispatchPointerEvent,
+  mockBoundingClientRect,
+} from "./utils/test-utils";
+import type { PanelResizeHandleProps } from "react-resizable-panels";
 
 describe("PanelResizeHandle", () => {
   let expectedWarnings: string[] = [];
@@ -67,47 +71,204 @@ describe("PanelResizeHandle", () => {
     expect(element.title).toBe("bar");
   });
 
+  function setupMockedGroup({
+    leftProps = {},
+    rightProps = {},
+  }: {
+    leftProps?: Partial<PanelResizeHandleProps>;
+    rightProps?: Partial<PanelResizeHandleProps>;
+  } = {}) {
+    act(() => {
+      root.render(
+        <PanelGroup direction="horizontal" id="test-group">
+          <Panel />
+          <PanelResizeHandle id="handle-left" tabIndex={1} {...leftProps} />
+          <Panel />
+          <PanelResizeHandle id="handle-right" tabIndex={2} {...rightProps} />
+          <Panel />
+        </PanelGroup>
+      );
+    });
+
+    const leftElement = container.querySelector(
+      '[data-panel-resize-handle-id="handle-left"]'
+    ) as HTMLElement;
+
+    const rightElement = container.querySelector(
+      '[data-panel-resize-handle-id="handle-right"]'
+    ) as HTMLElement;
+
+    // JSDom doesn't properly handle bounding rects
+    mockBoundingClientRect(leftElement, {
+      x: 50,
+      y: 0,
+      height: 50,
+      width: 2,
+    });
+    mockBoundingClientRect(rightElement, {
+      x: 100,
+      y: 0,
+      height: 50,
+      width: 2,
+    });
+
+    return {
+      leftElement,
+      rightElement,
+    };
+  }
+
   describe("callbacks", () => {
     describe("onDragging", () => {
-      it("should fire when dragging starts/stops", async () => {
+      it("should fire when dragging starts/stops", () => {
         const onDragging = jest.fn();
 
-        act(() => {
-          root.render(
-            <PanelGroup direction="horizontal">
-              <Panel />
-              <PanelResizeHandle
-                id="handle"
-                onDragging={onDragging}
-                tabIndex={123}
-                title="bar"
-              />
-              <Panel />
-            </PanelGroup>
-          );
+        const { leftElement } = setupMockedGroup({
+          leftProps: { onDragging },
         });
 
-        const handleElement = container.querySelector(
-          '[data-panel-resize-handle-id="handle"]'
-        ) as HTMLElement;
-
         act(() => {
-          dispatchPointerEvent("mouseover", handleElement);
+          dispatchPointerEvent("mousemove", leftElement);
         });
         expect(onDragging).not.toHaveBeenCalled();
 
         act(() => {
-          dispatchPointerEvent("mousedown", handleElement);
+          dispatchPointerEvent("mousedown", leftElement);
         });
         expect(onDragging).toHaveBeenCalledTimes(1);
         expect(onDragging).toHaveBeenCalledWith(true);
 
         act(() => {
-          dispatchPointerEvent("mouseup", handleElement);
+          dispatchPointerEvent("mouseup", leftElement);
         });
         expect(onDragging).toHaveBeenCalledTimes(2);
         expect(onDragging).toHaveBeenCalledWith(false);
       });
+
+      it("should only fire for the handle that has been dragged", () => {
+        const onDraggingLeft = jest.fn();
+        const onDraggingRight = jest.fn();
+
+        const { leftElement } = setupMockedGroup({
+          leftProps: { onDragging: onDraggingLeft },
+          rightProps: { onDragging: onDraggingRight },
+        });
+
+        act(() => {
+          dispatchPointerEvent("mousemove", leftElement);
+        });
+        expect(onDraggingLeft).not.toHaveBeenCalled();
+        expect(onDraggingRight).not.toHaveBeenCalled();
+
+        act(() => {
+          dispatchPointerEvent("mousedown", leftElement);
+        });
+        expect(onDraggingLeft).toHaveBeenCalledTimes(1);
+        expect(onDraggingLeft).toHaveBeenCalledWith(true);
+        expect(onDraggingRight).not.toHaveBeenCalled();
+
+        act(() => {
+          dispatchPointerEvent("mouseup", leftElement);
+        });
+        expect(onDraggingLeft).toHaveBeenCalledTimes(2);
+        expect(onDraggingLeft).toHaveBeenCalledWith(false);
+        expect(onDraggingRight).not.toHaveBeenCalled();
+      });
+    });
+  });
+
+  describe("data attributes", () => {
+    function verifyAttribute(
+      element: HTMLElement,
+      attributeName: string,
+      expectedValue: string | null
+    ) {
+      const actualValue = element.getAttribute(attributeName);
+      expect(actualValue).toBe(expectedValue);
+    }
+
+    it("should initialize with the correct props based attributes", () => {
+      const { leftElement, rightElement } = setupMockedGroup();
+
+      verifyAttribute(leftElement, "data-panel-group-id", "test-group");
+      verifyAttribute(leftElement, "data-resize-handle", "");
+      verifyAttribute(leftElement, "data-panel-group-direction", "horizontal");
+      verifyAttribute(leftElement, "data-panel-resize-handle-enabled", "true");
+      verifyAttribute(
+        leftElement,
+        "data-panel-resize-handle-id",
+        "handle-left"
+      );
+
+      verifyAttribute(rightElement, "data-panel-group-id", "test-group");
+      verifyAttribute(rightElement, "data-resize-handle", "");
+      verifyAttribute(rightElement, "data-panel-group-direction", "horizontal");
+      verifyAttribute(rightElement, "data-panel-resize-handle-enabled", "true");
+      verifyAttribute(
+        rightElement,
+        "data-panel-resize-handle-id",
+        "handle-right"
+      );
+    });
+
+    it("should update data-resize-handle-active and data-resize-handle-state when dragging starts/stops", () => {
+      const { leftElement, rightElement } = setupMockedGroup();
+      verifyAttribute(leftElement, "data-resize-handle-active", null);
+      verifyAttribute(rightElement, "data-resize-handle-active", null);
+      verifyAttribute(leftElement, "data-resize-handle-state", "inactive");
+      verifyAttribute(rightElement, "data-resize-handle-state", "inactive");
+
+      act(() => {
+        dispatchPointerEvent("mousemove", leftElement);
+      });
+      verifyAttribute(leftElement, "data-resize-handle-active", null);
+      verifyAttribute(rightElement, "data-resize-handle-active", null);
+      verifyAttribute(leftElement, "data-resize-handle-state", "hover");
+      verifyAttribute(rightElement, "data-resize-handle-state", "inactive");
+
+      act(() => {
+        dispatchPointerEvent("mousedown", leftElement);
+      });
+      verifyAttribute(leftElement, "data-resize-handle-active", "pointer");
+      verifyAttribute(rightElement, "data-resize-handle-active", null);
+      verifyAttribute(leftElement, "data-resize-handle-state", "drag");
+      verifyAttribute(rightElement, "data-resize-handle-state", "inactive");
+
+      act(() => {
+        dispatchPointerEvent("mouseup", leftElement);
+      });
+      verifyAttribute(leftElement, "data-resize-handle-active", null);
+      verifyAttribute(rightElement, "data-resize-handle-active", null);
+      verifyAttribute(leftElement, "data-resize-handle-state", "hover");
+      verifyAttribute(rightElement, "data-resize-handle-state", "inactive");
+
+      act(() => {
+        dispatchPointerEvent("mousemove", rightElement);
+      });
+      verifyAttribute(leftElement, "data-resize-handle-active", null);
+      verifyAttribute(rightElement, "data-resize-handle-active", null);
+      verifyAttribute(leftElement, "data-resize-handle-state", "inactive");
+      verifyAttribute(rightElement, "data-resize-handle-state", "hover");
+    });
+
+    it("should update data-resize-handle-active when focused", () => {
+      const { leftElement, rightElement } = setupMockedGroup();
+      verifyAttribute(leftElement, "data-resize-handle-active", null);
+      verifyAttribute(rightElement, "data-resize-handle-active", null);
+
+      act(() => {
+        leftElement.focus();
+      });
+      expect(document.activeElement).toBe(leftElement);
+      verifyAttribute(leftElement, "data-resize-handle-active", "keyboard");
+      verifyAttribute(rightElement, "data-resize-handle-active", null);
+
+      act(() => {
+        leftElement.blur();
+      });
+      expect(document.activeElement).not.toBe(leftElement);
+      verifyAttribute(leftElement, "data-resize-handle-active", null);
+      verifyAttribute(rightElement, "data-resize-handle-active", null);
     });
   });
 });
diff --git a/packages/react-resizable-panels/src/PanelResizeHandle.ts b/packages/react-resizable-panels/src/PanelResizeHandle.ts
index b6255704b..2f4450dd5 100644
--- a/packages/react-resizable-panels/src/PanelResizeHandle.ts
+++ b/packages/react-resizable-panels/src/PanelResizeHandle.ts
@@ -21,11 +21,11 @@ import {
   PointerHitAreaMargins,
   registerResizeHandle,
   ResizeHandlerAction,
-  ResizeHandlerState,
 } from "./PanelResizeHandleRegistry";
 import { assert } from "./utils/assert";
 
 export type PanelResizeHandleOnDragging = (isDragging: boolean) => void;
+export type ResizeHandlerState = "drag" | "hover" | "inactive";
 
 export type PanelResizeHandleProps = Omit<
   HTMLAttributes<keyof HTMLElementTagNameMap>,
@@ -109,37 +109,42 @@ export function PanelResizeHandle({
 
     const setResizeHandlerState = (
       action: ResizeHandlerAction,
-      state: ResizeHandlerState,
+      isActive: boolean,
       event: ResizeEvent
     ) => {
-      setState(state);
-
-      switch (action) {
-        case "down": {
-          startDragging(resizeHandleId, event);
-
-          const { onDragging } = callbacksRef.current;
-          if (onDragging) {
-            onDragging(true);
+      if (isActive) {
+        switch (action) {
+          case "down": {
+            setState("drag");
+
+            startDragging(resizeHandleId, event);
+
+            const { onDragging } = callbacksRef.current;
+            if (onDragging) {
+              onDragging(true);
+            }
+            break;
           }
-          break;
-        }
-        case "up": {
-          stopDragging();
+          case "move": {
+            setState("hover");
 
-          const { onDragging } = callbacksRef.current;
-          if (onDragging) {
-            onDragging(false);
+            resizeHandler(event);
+            break;
           }
-          break;
-        }
-      }
+          case "up": {
+            setState("hover");
+
+            stopDragging();
 
-      switch (state) {
-        case "drag": {
-          resizeHandler(event);
-          break;
+            const { onDragging } = callbacksRef.current;
+            if (onDragging) {
+              onDragging(false);
+            }
+            break;
+          }
         }
+      } else {
+        setState("inactive");
       }
     };
 
diff --git a/packages/react-resizable-panels/src/PanelResizeHandleRegistry.ts b/packages/react-resizable-panels/src/PanelResizeHandleRegistry.ts
index a7b14d1a8..37811b7a2 100644
--- a/packages/react-resizable-panels/src/PanelResizeHandleRegistry.ts
+++ b/packages/react-resizable-panels/src/PanelResizeHandleRegistry.ts
@@ -4,10 +4,9 @@ import { getResizeEventCoordinates } from "./utils/events/getResizeEventCoordina
 import { getInputType } from "./utils/getInputType";
 
 export type ResizeHandlerAction = "down" | "move" | "up";
-export type ResizeHandlerState = "drag" | "hover" | "inactive";
 export type SetResizeHandlerState = (
   action: ResizeHandlerAction,
-  state: ResizeHandlerState,
+  isActive: boolean,
   event: ResizeEvent
 ) => void;
 
@@ -93,21 +92,18 @@ function handlePointerDown(event: ResizeEvent) {
 function handlePointerMove(event: ResizeEvent) {
   const { x, y } = getResizeEventCoordinates(event);
 
-  if (isPointerDown) {
-    intersectingHandles.forEach((data) => {
-      const { setResizeHandlerState } = data;
-
-      setResizeHandlerState("move", "drag", event);
-    });
-
-    // Update cursor based on return value(s) from active handles
-    updateCursor();
-  } else {
+  if (!isPointerDown) {
+    // Recalculate intersecting handles whenever the pointer moves, except if it has already been pressed
+    // at that point, the handles may not move with the pointer (depending on constraints)
+    // but the same set of active handles should be locked until the pointer is released
     recalculateIntersectingHandles({ x, y });
-    updateResizeHandlerStates("move", event);
-    updateCursor();
   }
 
+  updateResizeHandlerStates("move", event);
+
+  // Update cursor based on return value(s) from active handles
+  updateCursor();
+
   if (intersectingHandles.length > 0) {
     event.preventDefault();
   }
@@ -250,14 +246,8 @@ function updateResizeHandlerStates(
   registeredResizeHandlers.forEach((data) => {
     const { setResizeHandlerState } = data;
 
-    if (intersectingHandles.includes(data)) {
-      if (isPointerDown) {
-        setResizeHandlerState(action, "drag", event);
-      } else {
-        setResizeHandlerState(action, "hover", event);
-      }
-    } else {
-      setResizeHandlerState(action, "inactive", event);
-    }
+    const isActive = intersectingHandles.includes(data);
+
+    setResizeHandlerState(action, isActive, event);
   });
 }
diff --git a/packages/react-resizable-panels/src/utils/test-utils.ts b/packages/react-resizable-panels/src/utils/test-utils.ts
index 4a787e3fc..5b0d8c6cf 100644
--- a/packages/react-resizable-panels/src/utils/test-utils.ts
+++ b/packages/react-resizable-panels/src/utils/test-utils.ts
@@ -47,6 +47,36 @@ export function expectToBeCloseToArray(
   }
 }
 
+export function mockBoundingClientRect(
+  element: HTMLElement,
+  rect: {
+    height: number;
+    width: number;
+    x: number;
+    y: number;
+  }
+) {
+  const { height, width, x, y } = rect;
+
+  Object.defineProperty(element, "getBoundingClientRect", {
+    configurable: true,
+    value: () =>
+      ({
+        bottom: y + height,
+        height,
+        left: x,
+        right: x + width,
+        toJSON() {
+          return "";
+        },
+        top: y,
+        width,
+        x,
+        y,
+      }) satisfies DOMRect,
+  });
+}
+
 export function mockPanelGroupOffsetWidthAndHeight(
   mockWidth = 1_000,
   mockHeight = 1_000