diff --git a/packages/svelte/src/internal/client/dom/blocks/portal.js b/packages/svelte/src/internal/client/dom/blocks/portal.js
index f935e9338a..c0d73687b2 100644
--- a/packages/svelte/src/internal/client/dom/blocks/portal.js
+++ b/packages/svelte/src/internal/client/dom/blocks/portal.js
@@ -1,16 +1,11 @@
 /** @import { Effect, Source, TemplateNode } from '#client' */
 /** @import { Batch } from '../../reactivity/batch.js' */
 import { DESTROYED, DESTROYING, HEAD_EFFECT } from '#client/constants';
+import { async_mode_flag } from '../../../flags/index.js';
 import { capture } from '../../reactivity/async.js';
-import { current_batch } from '../../reactivity/batch.js';
-import {
-	block,
-	branch,
-	destroy_effect,
-	move_effect,
-	render_effect
-} from '../../reactivity/effects.js';
-import { set, source } from '../../reactivity/sources.js';
+import { current_batch, eager_block_effects } from '../../reactivity/batch.js';
+import { block, branch, destroy_effect, move_effect } from '../../reactivity/effects.js';
+import { internal_set, source } from '../../reactivity/sources.js';
 import { active_effect, get, untrack } from '../../runtime.js';
 import {
 	hydrate_next,
@@ -80,28 +75,6 @@ function get_outlet_entry(key) {
 	return entry;
 }
 
-/**
- * Run `fn` now (during hydration, where synchronous timing is required for
- * claiming server-rendered content), or in a microtask otherwise. The latter
- * ensures that outlet (un)registrations - which can happen while a batch is
- * being committed - do not interfere with the commit by scheduling portal
- * updates (which would happen in a new batch) at the wrong moment.
- * @param {() => void} fn
- */
-function run_outside_batch(fn) {
-	if (hydrating) {
-		fn();
-	} else {
-		// TODO this is a hack to get around a (I think) general batch.js bug
-		// where setting state while flushing (render) effects can mess with
-		// #commit() of the earlier batch that runs afterwards, where roots
-		// would not be scheduled for other batches anymore because scheduling
-		// an effect might reach a branch that is already unclean, so scheduling
-		// thinks "oh we already have this root scheduled" (wrong because not in the context of that batch).
-		queue_micro_task(fn);
-	}
-}
-
 /**
  * Returns the node before which the content of a portal with the given
  * sequence number must be inserted, so that the contents of multiple portals
@@ -159,54 +132,60 @@ export function portal_outlet(node, get_id) {
 	if (hydrating) {
 		// `node` is the `<!--[-->` comment — advance to the `<!--portal:N-->` marker.
 		// Server-rendered content of `{#portal ...}` blocks comes right after it
-		// and is claimed by the corresponding blocks during hydration
+		// and is claimed by the corresponding blocks during hydration.
 		anchor = hydrate_next();
 	}
 
 	/** @type {Outlet} */
 	var outlet = { anchor, claim: hydrating ? anchor : null, items: [] };
 
-	// TODO this should be a block effect so it runs during traversal. The way it's right now
-	// it means that a #portal block with async work will have that async work not coordinated
-	// if it's instantiated through this @portal for the first time.
-	render_effect(() => {
+	// A block effect, so that (un)registration happens during batch traversal.
+	// Portals rendering into this outlet are scheduled and re-run within the
+	// same traversal (via `internal_set`, which schedules reactions into the
+	// current batch) - that way, any async work their content contains is
+	// discovered before the batch commits, and the batch waits for it.
+	block(() => {
+		const effect = /** @type {Effect} */ (active_effect);
 		const id = get_id();
 		if (id == null) return;
 
 		const entry = get_outlet_entry(id);
 
-		var registered = false;
-		var cancelled = false;
+		internal_set(entry.outlets, [...entry.outlets.v, outlet]);
 
-		const register = () => {
-			if (cancelled) return;
-			registered = true;
-
-			set(
-				entry.outlets,
-				untrack(() => [...get(entry.outlets), outlet])
-			);
-
-			// during hydration, portals that were created before this outlet claim
-			// their server-rendered content now, while the hydration position is known
-			for (const render of entry.pending) {
-				render(outlet);
-			}
-		};
+		// During hydration, portals that were created before this outlet claim
+		// their server-rendered content now, while the hydration position is known.
+		for (const render of entry.pending) {
+			render(outlet);
+		}
 
 		const unregister = () => {
-			cancelled = true;
-			if (!registered) return;
-
-			set(
+			internal_set(
 				entry.outlets,
-				untrack(() => get(entry.outlets).filter((o) => o !== outlet))
+				entry.outlets.v.filter((o) => o !== outlet)
 			);
 		};
 
-		run_outside_batch(register);
-
-		return () => run_outside_batch(unregister);
+		return () => {
+			if ((effect.f & (DESTROYED | DESTROYING)) !== 0) {
+				// The outlet is being destroyed, which happens while a batch is being
+				// committed. Unregistering right away would schedule the affected
+				// portals into a new batch mid-commit, interfering with how the
+				// committing batch reruns effects of other in-flight batches, so
+				// defer it (the DOM is already correct: portaled content is removed
+				// together with the outlet, or by the portals' own cleanup)
+
+				// TODO this feels like a hack to get around a (I think) general batch.js bug
+				// where setting state while committing + flushing (render) effects can mess with
+				// rebase of the earlier batches in #commit() that runs afterwards, where roots
+				// would not be scheduled for other batches anymore because scheduling
+				// an effect might reach a branch that is already unclean, so scheduling
+				// thinks "oh we already have this root scheduled" (wrong because not in the context of that batch).
+				queue_micro_task(unregister);
+			} else {
+				unregister();
+			}
+		};
 	});
 
 	if (hydrating) {
@@ -434,7 +413,9 @@ export function portal(get_target, content) {
 		// The outlets for this batch's key may have changed since the batch last
 		// ran (an outlet can be (un)registered by another batch, without this
 		// block necessarily re-running within this batch), so the target
-		// selection is computed from the now-committed state
+		// selection is computed from this batch's view of the world at commit
+		// time. The read must be batch-aware (`get` rather than `.v`), because
+		// other in-flight batches may have eagerly (un)registered outlets
 		/** @type {Set<Outlet | Element>} */
 		var targets = new Set();
 
@@ -442,7 +423,9 @@ export function portal(get_target, content) {
 			if (target instanceof Element) {
 				targets.add(target);
 			} else {
-				for (var outlet of get_outlet_entry(target).outlets.v) {
+				var outlets = untrack(() => get(get_outlet_entry(target).outlets));
+
+				for (var outlet of outlets) {
 					targets.add(outlet);
 				}
 			}
@@ -485,7 +468,15 @@ export function portal(get_target, content) {
 
 		var target = get_target();
 		var batch = /** @type {Batch} */ (current_batch);
-		var defer = should_defer_append();
+		// Unlike other blocks (whose fresh content is always contained by the
+		// parent branch being created (at mount, or offscreen)) a portal renders
+		// its content outside its own subtree, potentially into DOM that is
+		// already visible. Insertion is therefore deferred until the batch
+		// commits even on the block's first run (which `should_defer_append`
+		// alone would treat as an immediate append), so that content never
+		// appears before the rest of the batch.
+		var defer =
+			should_defer_append() || (async_mode_flag && !hydrating && eager_block_effects === null);
 
 		/** @type {Set<Outlet | Element>} */
 		var targets = new Set();
@@ -528,7 +519,7 @@ export function portal(get_target, content) {
 				// an outlet with our key may appear later during this hydration
 				// pass (`{#portal ...}` before `{@portal ...}` in the markup).
 				// Register a callback so it can have us claim our server-rendered
-				// content at its position
+				// content at its position.
 				var entry = get_outlet_entry(target);
 				var restore = capture();
 
diff --git a/packages/svelte/src/internal/client/reactivity/batch.js b/packages/svelte/src/internal/client/reactivity/batch.js
index 7d14b80519..cb493d805c 100644
--- a/packages/svelte/src/internal/client/reactivity/batch.js
+++ b/packages/svelte/src/internal/client/reactivity/batch.js
@@ -304,9 +304,6 @@ export class Batch {
 			this.schedule(e);
 		}
 
-		const roots = this.#roots;
-		this.#roots = [];
-
 		this.apply();
 
 		/** @type {Effect[]} */
@@ -321,20 +318,29 @@ export class Batch {
 		 */
 		var updates = (legacy_updates = []);
 
-		for (const root of roots) {
-			try {
-				this.#traverse(root, effects, render_effects);
-			} catch (e) {
-				reset_all(root);
-				// If there's no async work left, this branch is now dead and needs
-				// to be discarded to not become a zombie that is never cleaned up.
-				// See https://github.com/sveltejs/svelte/issues/18221#issuecomment-4497918414
-				// for a (non-minimal) reproduction that demonstrates a case where this is necessary
-				// to not get follow-up false-positives via "batch has scheduled roots" invariant errors.
-				if (!this.#is_deferred()) this.discard();
-				throw e;
+		do {
+			const roots = this.#roots;
+			this.#roots = [];
+
+			for (const root of roots) {
+				try {
+					this.#traverse(root, effects, render_effects);
+				} catch (e) {
+					reset_all(root);
+					// If there's no async work left, this branch is now dead and needs
+					// to be discarded to not become a zombie that is never cleaned up.
+					// See https://github.com/sveltejs/svelte/issues/18221#issuecomment-4497918414
+					// for a (non-minimal) reproduction that demonstrates a case where this is necessary
+					// to not get follow-up false-positives via "batch has scheduled roots" invariant errors.
+					if (!this.#is_deferred()) this.discard();
+					throw e;
+				}
 			}
-		}
+
+			// If state was set during traversal, re-traverse right away to avoid
+			// tearing: e.g. an if block with async work inside could've been toggled,
+			// and without re-traversal we might wrongfully commit/render if there's no other async work left.
+		} while (this.#roots.length > 0);
 
 		// any writes should take effect in a subsequent batch
 		current_batch = null;
diff --git a/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-1/_config.js b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-1/_config.js
new file mode 100644
index 0000000000..7eda1397ea
--- /dev/null
+++ b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-1/_config.js
@@ -0,0 +1,16 @@
+import { tick } from 'svelte';
+import { test } from '../../test';
+
+export default test({
+	async test({ assert, target }) {
+		const [toggle, resolve] = target.querySelectorAll('button');
+
+		toggle.click();
+		await tick();
+		assert.htmlEqual(target.innerHTML, `<button>toggle</button> <button>resolve</button> a`);
+
+		resolve.click();
+		await tick();
+		assert.htmlEqual(target.innerHTML, `<button>toggle</button> <button>resolve</button> b b`);
+	}
+});
diff --git a/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-1/main.svelte b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-1/main.svelte
new file mode 100644
index 0000000000..64f425edb7
--- /dev/null
+++ b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-1/main.svelte
@@ -0,0 +1,23 @@
+<script>
+	let outletKey = $state('a');
+
+	let queued = [];
+
+	function push(v) {
+		return new Promise((resolve) => {
+			queued.push(() => resolve(v));
+		});
+	}
+</script>
+
+<button onclick={() => outletKey = outletKey === 'a' ? 'b' : 'a'}>toggle</button>
+<button onclick={() => queued.shift()?.()}>resolve</button>
+
+{#portal 'b'}
+	{await push('b')}
+{/portal}
+
+{outletKey}
+{#if outletKey === 'b'}
+	{@portal outletKey}
+{/if}
diff --git a/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-2/_config.js b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-2/_config.js
new file mode 100644
index 0000000000..7eda1397ea
--- /dev/null
+++ b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-2/_config.js
@@ -0,0 +1,16 @@
+import { tick } from 'svelte';
+import { test } from '../../test';
+
+export default test({
+	async test({ assert, target }) {
+		const [toggle, resolve] = target.querySelectorAll('button');
+
+		toggle.click();
+		await tick();
+		assert.htmlEqual(target.innerHTML, `<button>toggle</button> <button>resolve</button> a`);
+
+		resolve.click();
+		await tick();
+		assert.htmlEqual(target.innerHTML, `<button>toggle</button> <button>resolve</button> b b`);
+	}
+});
diff --git a/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-2/main.svelte b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-2/main.svelte
new file mode 100644
index 0000000000..7bd2038479
--- /dev/null
+++ b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-2/main.svelte
@@ -0,0 +1,21 @@
+<script>
+	let portal_key = $state('a');
+
+	let queued = [];
+
+	function push(v) {
+		return new Promise((resolve) => {
+			queued.push(() => resolve(v));
+		});
+	}
+</script>
+
+<button onclick={() => portal_key = portal_key === 'a' ? 'b' : 'a'}>toggle</button>
+<button onclick={() => queued.shift()?.()}>resolve</button>
+
+{@portal 'b'}
+
+{portal_key}
+{#portal portal_key}
+	{await push('b')}
+{/portal}
diff --git a/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-3/_config.js b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-3/_config.js
new file mode 100644
index 0000000000..8d55bcc948
--- /dev/null
+++ b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-3/_config.js
@@ -0,0 +1,21 @@
+import { tick } from 'svelte';
+import { test } from '../../test';
+
+export default test({
+	async test({ assert, target }) {
+		const [show, resolve] = target.querySelectorAll('button');
+
+		show.click();
+		await tick();
+		// the batch is blocked on the portal content's async work — nothing
+		// (including the synchronous parts of the portal content) may appear yet
+		assert.htmlEqual(target.innerHTML, `<button>show</button> <button>resolve</button> false`);
+
+		resolve.click();
+		await tick();
+		assert.htmlEqual(
+			target.innerHTML,
+			`<button>show</button> <button>resolve</button> <h1>static</h1> async true`
+		);
+	}
+});
diff --git a/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-3/main.svelte b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-3/main.svelte
new file mode 100644
index 0000000000..2b7d09ac68
--- /dev/null
+++ b/packages/svelte/tests/runtime-runes/samples/async-portal-coordination-3/main.svelte
@@ -0,0 +1,24 @@
+<script>
+	let show = $state(false);
+
+	let queued = [];
+
+	function push(v) {
+		return new Promise((resolve) => {
+			queued.push(() => resolve(v));
+		});
+	}
+</script>
+
+<button onclick={() => show = true}>show</button>
+<button onclick={() => queued.shift()?.()}>resolve</button>
+
+{@portal 'target'}
+
+{show}
+{#if show}
+	{#portal 'target'}
+		<h1>static</h1>
+		{await push('async')}
+	{/portal}
+{/if}