diff --git a/src/browser/js/Caller.zig b/src/browser/js/Caller.zig
index 297d4ac1..9ecd65b2 100644
--- a/src/browser/js/Caller.zig
+++ b/src/browser/js/Caller.zig
@@ -40,8 +40,8 @@ prev_context: *Context,
 
 // Takes the raw v8 isolate and extracts the context from it.
 pub fn init(self: *Caller, v8_isolate: *v8.Isolate) void {
-    const v8_context = v8.v8__Isolate__GetCurrentContext(v8_isolate).?;
-    initWithContext(self, Context.fromC(v8_context), v8_context);
+    const ctx, const v8_context = Context.fromIsolate(.{ .handle = v8_isolate });
+    initWithContext(self, ctx, v8_context);
 }
 
 fn initWithContext(self: *Caller, ctx: *Context, v8_context: *const v8.Context) void {
@@ -537,9 +537,7 @@ pub const Function = struct {
 
     pub fn call(comptime T: type, info_handle: *const v8.FunctionCallbackInfo, func: anytype, comptime opts: Opts) void {
         const v8_isolate = v8.v8__FunctionCallbackInfo__GetIsolate(info_handle).?;
-        const v8_context = v8.v8__Isolate__GetCurrentContext(v8_isolate).?;
-
-        const ctx = Context.fromC(v8_context);
+        const ctx, const v8_context = Context.fromIsolate(.{ .handle = v8_isolate });
         const info = FunctionCallbackInfo{ .handle = info_handle };
 
         var hs: js.HandleScope = undefined;
diff --git a/src/browser/js/Context.zig b/src/browser/js/Context.zig
index ea1b6f7a..da7362aa 100644
--- a/src/browser/js/Context.zig
+++ b/src/browser/js/Context.zig
@@ -119,12 +119,22 @@ const ModuleEntry = struct {
     resolver_promise: ?js.Promise.Global = null,
 };
 
-pub fn fromC(c_context: *const v8.Context) *Context {
+pub fn fromC(c_context: *const v8.Context) ?*Context {
     return @ptrCast(@alignCast(v8.v8__Context__GetAlignedPointerFromEmbedderData(c_context, 1)));
 }
 
-pub fn fromIsolate(isolate: js.Isolate) *Context {
-    return fromC(v8.v8__Isolate__GetCurrentContext(isolate.handle).?);
+/// Returns the Context and v8::Context for the given isolate.
+/// If the current context is from a destroyed Context (e.g., navigated-away iframe),
+/// falls back to the incumbent context (the calling context).
+pub fn fromIsolate(isolate: js.Isolate) struct { *Context, *const v8.Context } {
+    const v8_context = v8.v8__Isolate__GetCurrentContext(isolate.handle).?;
+    if (fromC(v8_context)) |ctx| {
+        return .{ ctx, v8_context };
+    }
+    // The current context's Context struct has been freed (e.g., iframe navigated away).
+    // Fall back to the incumbent context (the calling context).
+    const v8_incumbent = v8.v8__Isolate__GetIncumbentContext(isolate.handle).?;
+    return .{ fromC(v8_incumbent).?, v8_incumbent };
 }
 
 pub fn deinit(self: *Context) void {
@@ -155,6 +165,11 @@ pub fn deinit(self: *Context) void {
 
     self.session.releaseOrigin(self.origin);
 
+    // Clear the embedder data so that if V8 keeps this context alive
+    // (because objects created in it are still referenced), we don't
+    // have a dangling pointer to our freed Context struct.
+    v8.v8__Context__SetAlignedPointerInEmbedderData(entered.handle, 1, null);
+
     v8.v8__Global__Reset(&self.handle);
     env.isolate.notifyContextDisposed();
     // There can be other tasks associated with this context that we need to
@@ -255,7 +270,7 @@ pub fn toLocal(self: *Context, global: anytype) js.Local.ToLocalReturnType(@Type
 }
 
 pub fn getIncumbent(self: *Context) *Page {
-    return fromC(v8.v8__Isolate__GetIncumbentContext(self.env.isolate.handle).?).page;
+    return fromC(v8.v8__Isolate__GetIncumbentContext(self.env.isolate.handle).?).?.page;
 }
 
 pub fn stringToPersistedFunction(
@@ -479,7 +494,7 @@ fn resolveModuleCallback(
 ) callconv(.c) ?*const v8.Module {
     _ = import_attributes;
 
-    const self = fromC(c_context.?);
+    const self = fromC(c_context.?).?;
     const local = js.Local{
         .ctx = self,
         .handle = c_context.?,
@@ -512,7 +527,7 @@ pub fn dynamicModuleCallback(
     _ = host_defined_options;
     _ = import_attrs;
 
-    const self = fromC(c_context.?);
+    const self = fromC(c_context.?).?;
     const local = js.Local{
         .ctx = self,
         .handle = c_context.?,
@@ -559,7 +574,7 @@ pub fn dynamicModuleCallback(
 
 pub fn metaObjectCallback(c_context: ?*v8.Context, c_module: ?*v8.Module, c_meta: ?*v8.Value) callconv(.c) void {
     // @HandleScope  implement this without a fat context/local..
-    const self = fromC(c_context.?);
+    const self = fromC(c_context.?).?;
     var local = js.Local{
         .ctx = self,
         .handle = c_context.?,
diff --git a/src/browser/js/Env.zig b/src/browser/js/Env.zig
index 1ac9e6b3..09117eb0 100644
--- a/src/browser/js/Env.zig
+++ b/src/browser/js/Env.zig
@@ -497,13 +497,13 @@ pub fn terminate(self: *const Env) void {
 fn promiseRejectCallback(message_handle: v8.PromiseRejectMessage) callconv(.c) void {
     const promise_handle = v8.v8__PromiseRejectMessage__GetPromise(&message_handle).?;
     const v8_isolate = v8.v8__Object__GetIsolate(@ptrCast(promise_handle)).?;
-    const js_isolate = js.Isolate{ .handle = v8_isolate };
-    const ctx = Context.fromIsolate(js_isolate);
+    const isolate = js.Isolate{ .handle = v8_isolate };
+    const ctx, const v8_context = Context.fromIsolate(isolate);
 
     const local = js.Local{
         .ctx = ctx,
-        .isolate = js_isolate,
-        .handle = v8.v8__Isolate__GetCurrentContext(v8_isolate).?,
+        .isolate = isolate,
+        .handle = v8_context,
         .call_arena = ctx.call_arena,
     };