diff --git a/l10n/messages.pot b/l10n/messages.pot
index 59eba91aa8..f45235049d 100644
--- a/l10n/messages.pot
+++ b/l10n/messages.pot
@@ -332,6 +332,9 @@ msgstr ""
 msgid "Search for time zone"
 msgstr ""
 
+msgid "Search in app…"
+msgstr ""
+
 msgid "Search results"
 msgstr ""
 
diff --git a/src/components/NcAppNavigation/NcAppNavigation.vue b/src/components/NcAppNavigation/NcAppNavigation.vue
index c877060531..b150bd0023 100644
--- a/src/components/NcAppNavigation/NcAppNavigation.vue
+++ b/src/components/NcAppNavigation/NcAppNavigation.vue
@@ -33,6 +33,103 @@ emit('toggle-navigation', {
 })
 ```
 
+#### With in-app search
+
+```vue
+<template>
+	<div class="styleguide-wrapper">
+		<NcContent app-name="styleguide-app-navigation" class="content-styleguidist">
+			<NcAppNavigation show-search :search.sync="searchQuery">
+				<template #search-actions>
+					<NcActionButton>
+						<template #icon>
+							<IconFilter :size="20" />
+						</template>
+						Filter
+					</NcActionButton>
+					<NcActionButton>
+						<template #icon>
+							<IconSearchGlobal :size="20" />
+						</template>
+						Search globally
+					</NcActionButton>
+				</template>
+				<template #list>
+					<NcAppNavigationItem name="First navigation entry">
+						<template #icon>
+							<IconStar :size="20" />
+						</template>
+					</NcAppNavigationItem>
+					<NcAppNavigationItem name="Second navigation entry">
+						<template #icon>
+							<IconStar :size="20" />
+						</template>
+					</NcAppNavigationItem>
+				</template>
+				</NcAppNavigation>
+			<NcAppContent>
+				<ul class="fake-content">
+					<li>Search query: {{ searchQuery }}</li>
+					<li v-for="(item, index) in items" :key="index">
+						{{ item }}
+					</li>
+				</ul>
+			</NcAppContent>
+		</NcContent>
+	</div>
+</template>
+<script>
+import IconFilter from 'vue-material-design-icons/Filter.vue'
+import IconSearchGlobal from 'vue-material-design-icons/CloudSearch.vue'
+import IconStar from 'vue-material-design-icons/Star.vue'
+
+const exampleItem = ['Mary', 'Patricia', 'James', 'Michael']
+
+export default {
+	components: {
+		IconFilter,
+		IconSearchGlobal,
+		IconStar,
+	},
+
+	data() {
+		return {
+			searchQuery: '',
+		}
+	},
+
+	computed: {
+		items() {
+			return exampleItem.filter((item) => item.toLocaleLowerCase().includes(this.searchQuery.toLocaleLowerCase()))
+		},
+	},
+}
+</script>
+<style scoped>
+/* This styles just mock NcContent and NcAppContent */
+.content-styleguidist {
+	position: relative !important;
+	margin: 0 !important;
+	/* prvent jumping */
+	min-height: 200px;
+}
+
+.content-styleguidist > * {
+	height: auto;
+}
+
+.fake-content {
+	padding: var(--app-navigation-padding);
+	padding-top: calc(2 * var(--app-navigation-padding) + var(--default-clickable-area));
+}
+
+.styleguide-wrapper {
+	background-color: var(--color-background-plain);
+	padding: var(--body-container-margin);
+}
+</style>
+```
+
 </docs>
 
 <template>
@@ -47,6 +144,17 @@ emit('toggle-navigation', {
 			:inert="!open || undefined"
 			@keydown.esc="handleEsc">
 			<div class="app-navigation__body" :class="{ 'app-navigation__body--no-list': !$scopedSlots.list }">
+				<NcAppNavigationSearch v-if="showSearch"
+					:label="searchLabel || undefined"
+					:no-inline-actions="noSearchInlineActions"
+					:value="search"
+					@update:value="$emit('update:search', $event)">
+					<template #actions>
+						<!-- @slot Optional NcAction* to show next to the search input -->
+						<slot name="search-actions" />
+					</template>
+				</NcAppNavigationSearch>
+
 				<!-- The main content of the navigation. If no list is passed to the #list slot, stretched vertically. -->
 				<slot />
 			</div>
@@ -69,8 +177,9 @@ import { getTrapStack } from '../../utils/focusTrap.js'
 import { emit, subscribe, unsubscribe } from '@nextcloud/event-bus'
 import { createFocusTrap } from 'focus-trap'
 
-import NcAppNavigationToggle from '../NcAppNavigationToggle/index.js'
 import NcAppNavigationList from '../NcAppNavigationList/index.js'
+import NcAppNavigationSearch from './NcAppNavigationSearch.vue'
+import NcAppNavigationToggle from '../NcAppNavigationToggle/index.js'
 import Vue from 'vue'
 
 export default {
@@ -78,6 +187,7 @@ export default {
 
 	components: {
 		NcAppNavigationList,
+		NcAppNavigationSearch,
 		NcAppNavigationToggle,
 	},
 
@@ -105,6 +215,38 @@ export default {
 			type: String,
 			default: '',
 		},
+
+		/**
+		 * If set an in-app search is shown as the first entry
+		 */
+		showSearch: {
+			type: Boolean,
+			default: false,
+		},
+
+		/**
+		 * The current search query
+		 */
+		search: {
+			type: String,
+			default: '',
+		},
+
+		/**
+		 * Label of in-app search input
+		 */
+		searchLabel: {
+			type: String,
+			default: null,
+		},
+
+		/**
+		 * Force a menu if there is more than one search action
+		 */
+		noSearchInlineActions: {
+			type: Boolean,
+			default: false,
+		},
 	},
 
 	setup() {
diff --git a/src/components/NcAppNavigation/NcAppNavigationSearch.vue b/src/components/NcAppNavigation/NcAppNavigationSearch.vue
new file mode 100644
index 0000000000..5f69ce76fd
--- /dev/null
+++ b/src/components/NcAppNavigation/NcAppNavigationSearch.vue
@@ -0,0 +1,126 @@
+<!--
+  - SPDX-FileCopyrightText: 2024 Nextcloud GmbH and Nextcloud contributors
+  - SPDX-License-Identifier: AGPL-3.0-or-later
+-->
+<template>
+	<div class="app-navigation-search"
+		:class="{
+			'app-navigation-search--has-actions': hasActions(),
+		}">
+		<NcInputField ref="inputElement"
+			:aria-label="label"
+			class="app-navigation-search__input"
+			label-outside
+			:placeholder="label"
+			show-trailing-button
+			:trailing-button-label="t('Clear search')"
+			type="search"
+			:value="value"
+			@update:value="$emit('update:value', $event)"
+			@trailing-button-click="onCloseSearch">
+			<template #trailing-button-icon>
+				<IconClose :size="20" />
+			</template>
+		</NcInputField>
+		<Transition v-if="hasActions()" name="slide-fade">
+			<NcActions v-show="showActions"
+				ref="actions"
+				class="app-navigation-search__actions"
+				:inline="noInlineActions ? 0 : 1">
+				<slot name="actions" />
+			</NcActions>
+		</Transition>
+	</div>
+</template>
+
+<script setup>
+import { useFocusWithin } from '@vueuse/core'
+import { ref, nextTick, useSlots, watch } from 'vue'
+import { t } from '../../l10n.js'
+
+import IconClose from 'vue-material-design-icons/Close.vue'
+import NcInputField from '../NcInputField/NcInputField.vue'
+
+defineProps({
+	/**
+	 * Current search input
+	 */
+	value: {
+		type: String,
+		default: '',
+	},
+	/**
+	 * Text used to label the search input
+	 */
+	label: {
+		type: String,
+		default: t('Search in app…'),
+	},
+	/**
+	 * Disable inline actions forcing a menu if more than one action is provided
+	 */
+	noInlineActions: {
+		type: Boolean,
+		default: false,
+	},
+})
+
+const emit = defineEmits(['update:value'])
+const slots = useSlots()
+
+const inputElement = ref()
+const { focused: inputHasFocus } = useFocusWithin(inputElement)
+
+/**
+ * @type {import('vue').Ref<import('vue').ComponentPublicInstance>}
+ */
+const actions = ref()
+const hasActions = () => !!slots.actions
+const showActions = ref(true)
+watch(inputHasFocus, () => {
+	showActions.value = !inputHasFocus.value
+})
+
+/**
+ * Handle close the search
+ */
+function onCloseSearch() {
+	emit('update:value', '')
+	if (hasActions()) {
+		showActions.value = true
+		nextTick(() => actions.value.$el.querySelector('button').focus())
+	}
+}
+</script>
+
+<style scoped lang="scss">
+.app-navigation-search {
+	display: flex;
+	gap: var(--app-navigation-padding);
+	padding: var(--app-navigation-padding);
+
+	&--has-actions &__input {
+		flex-grow: 1;
+		z-index: 3;
+	}
+
+	&__actions {
+		margin-inline-start: 0;
+	}
+
+	&__input {
+		// This is a fallback for legacy version (Nextcloud 29 and older) so that we keep the pill like design there
+		--input-border-radius: var(--borer-radius-element, var(--border-radius-pill)) !important;
+	}
+}
+
+.slide-fade-enter-active,
+.slide-fade-leave-active {
+	transition: margin-inline-start var(--animation-quick);
+}
+
+.slide-fade-enter,
+.slide-fade-leave-to {
+	margin-inline-start: calc(-1 * var(--default-clickable-area));
+}
+</style>
diff --git a/styleguide.config.js b/styleguide.config.js
index 8113ead5cf..efec115b87 100644
--- a/styleguide.config.js
+++ b/styleguide.config.js
@@ -186,6 +186,7 @@ module.exports = async () => {
 									'src/components/NcAppNavigation*/*.vue',
 								],
 								ignore: [
+									'src/components/NcAppNavigation/NcAppNavigationSearch.vue',
 									'src/components/NcAppNavigationItem/NcAppNavigationIconCollapsible.vue',
 									'src/components/NcAppNavigationItem/NcInputConfirmCancel.vue',
 								],