diff --git a/crates/matrix-sdk-base/src/event_cache/store/media/media_service.rs b/crates/matrix-sdk-base/src/event_cache/store/media/media_service.rs
index 8bd183adb..508eb3246 100644
--- a/crates/matrix-sdk-base/src/event_cache/store/media/media_service.rs
+++ b/crates/matrix-sdk-base/src/event_cache/store/media/media_service.rs
@@ -15,9 +15,14 @@
 use std::{fmt, sync::Arc};
 
 use async_trait::async_trait;
-use matrix_sdk_common::{locks::Mutex, AsyncTraitDeps};
+use matrix_sdk_common::{
+    executor::{spawn, JoinHandle},
+    locks::Mutex,
+    AsyncTraitDeps, SendOutsideWasm, SyncOutsideWasm,
+};
 use ruma::{time::SystemTime, MxcUri};
 use tokio::sync::Mutex as AsyncMutex;
+use tracing::error;
 
 use super::MediaRetentionPolicy;
 use crate::{event_cache::store::EventCacheStoreError, media::MediaRequestParameters};
@@ -41,6 +46,15 @@ struct MediaServiceInner<Time: TimeProvider = DefaultTimeProvider> {
 
     /// A mutex to ensure a single cleanup is running at a time.
     cleanup_guard: AsyncMutex<()>,
+
+    /// The time of the last media cache cleanup.
+    last_media_cleanup_time: Mutex<Option<SystemTime>>,
+
+    /// The [`JoinHandle`] for an automatic media cleanup task.
+    ///
+    /// Used to ensure that only one automatic cleanup is running at a time, and
+    /// to stop the cleanup when the [`MediaServiceInner`] is dropped.
+    automatic_media_cleanup_join_handle: Mutex<Option<JoinHandle<()>>>,
 }
 
 impl MediaService {
@@ -61,7 +75,7 @@ impl Default for MediaService {
 
 impl<Time> MediaService<Time>
 where
-    Time: TimeProvider,
+    Time: TimeProvider + 'static,
 {
     /// Construct a new `MediaService` with the given `TimeProvider` and an
     /// empty `MediaRetentionPolicy`.
@@ -70,6 +84,8 @@ where
             time_provider,
             policy: Mutex::new(MediaRetentionPolicy::empty()),
             cleanup_guard: AsyncMutex::new(()),
+            last_media_cleanup_time: Mutex::new(None),
+            automatic_media_cleanup_join_handle: Mutex::new(None),
         };
 
         Self { inner: Arc::new(inner) }
@@ -83,10 +99,18 @@ where
     /// # Arguments
     ///
     /// * `policy` - The `MediaRetentionPolicy` that was persisted in the store.
-    pub fn restore(&self, policy: Option<MediaRetentionPolicy>) {
+    pub fn restore(
+        &self,
+        policy: Option<MediaRetentionPolicy>,
+        last_media_cleanup_time: Option<SystemTime>,
+    ) {
         if let Some(policy) = policy {
             *self.inner.policy.lock() = policy;
         }
+
+        if let Some(time) = last_media_cleanup_time {
+            *self.inner.last_media_cleanup_time.lock() = Some(time);
+        }
     }
 
     /// Get the current time from the inner [`TimeProvider`].
@@ -101,7 +125,7 @@ where
     /// * `store` - The `EventCacheStoreMedia`.
     ///
     /// * `policy` - The `MediaRetentionPolicy` to use.
-    pub async fn set_media_retention_policy<Store: EventCacheStoreMedia>(
+    pub async fn set_media_retention_policy<Store: EventCacheStoreMedia + 'static>(
         &self,
         store: &Store,
         policy: MediaRetentionPolicy,
@@ -110,6 +134,8 @@ where
 
         *self.inner.policy.lock() = policy;
 
+        self.maybe_spawn_automatic_media_cache_cleanup(store, self.now());
+
         Ok(())
     }
 
@@ -130,7 +156,7 @@ where
     ///
     /// * `ignore_policy` - Whether the current `MediaRetentionPolicy` should be
     ///   ignored.
-    pub async fn add_media_content<Store: EventCacheStoreMedia>(
+    pub async fn add_media_content<Store: EventCacheStoreMedia + 'static>(
         &self,
         store: &Store,
         request: &MediaRequestParameters,
@@ -146,7 +172,14 @@ where
             return Ok(());
         }
 
-        store.add_media_content_inner(request, content, self.now(), policy, ignore_policy).await
+        let current_time = self.now();
+        store
+            .add_media_content_inner(request, content, current_time, policy, ignore_policy)
+            .await?;
+
+        self.maybe_spawn_automatic_media_cache_cleanup(store, current_time);
+
+        Ok(())
     }
 
     /// Set whether the current [`MediaRetentionPolicy`] should be ignored for
@@ -178,12 +211,17 @@ where
     /// * `store` - The `EventCacheStoreMedia`.
     ///
     /// * `request` - The `MediaRequestParameters` of the file.
-    pub async fn get_media_content<Store: EventCacheStoreMedia>(
+    pub async fn get_media_content<Store: EventCacheStoreMedia + 'static>(
         &self,
         store: &Store,
         request: &MediaRequestParameters,
     ) -> Result<Option<Vec<u8>>, Store::Error> {
-        store.get_media_content_inner(request, self.now()).await
+        let current_time = self.now();
+        let content = store.get_media_content_inner(request, current_time).await?;
+
+        self.maybe_spawn_automatic_media_cache_cleanup(store, current_time);
+
+        Ok(content)
     }
 
     /// Get a media file's content associated to an `MxcUri` from the
@@ -194,12 +232,17 @@ where
     /// * `store` - The `EventCacheStoreMedia`.
     ///
     /// * `uri` - The `MxcUri` of the media file.
-    pub async fn get_media_content_for_uri<Store: EventCacheStoreMedia>(
+    pub async fn get_media_content_for_uri<Store: EventCacheStoreMedia + 'static>(
         &self,
         store: &Store,
         uri: &MxcUri,
     ) -> Result<Option<Vec<u8>>, Store::Error> {
-        store.get_media_content_for_uri_inner(uri, self.now()).await
+        let current_time = self.now();
+        let content = store.get_media_content_for_uri_inner(uri, current_time).await?;
+
+        self.maybe_spawn_automatic_media_cache_cleanup(store, current_time);
+
+        Ok(content)
     }
 
     /// Clean up the media cache with the current `MediaRetentionPolicy`.
@@ -212,6 +255,14 @@ where
     pub async fn clean_up_media_cache<Store: EventCacheStoreMedia>(
         &self,
         store: &Store,
+    ) -> Result<(), Store::Error> {
+        self.clean_up_media_cache_inner(store, self.now()).await
+    }
+
+    async fn clean_up_media_cache_inner<Store: EventCacheStoreMedia>(
+        &self,
+        store: &Store,
+        current_time: SystemTime,
     ) -> Result<(), Store::Error> {
         let Ok(_guard) = self.inner.cleanup_guard.try_lock() else {
             // There is another ongoing cleanup.
@@ -225,7 +276,56 @@ where
             return Ok(());
         }
 
-        store.clean_up_media_cache_inner(policy, self.now()).await
+        store.clean_up_media_cache_inner(policy, current_time).await?;
+
+        *self.inner.last_media_cleanup_time.lock() = Some(current_time);
+
+        Ok(())
+    }
+
+    /// Spawn an automatic media cache cleanup, according to the media retention
+    /// policy.
+    ///
+    /// A cleanup will be spawned if:
+    /// * The media retention policy's `cleanup_frequency` is set and enough
+    ///   time has passed since the last cleanup.
+    /// * No other cleanup is running,
+    fn maybe_spawn_automatic_media_cache_cleanup<Store: EventCacheStoreMedia + 'static>(
+        &self,
+        store: &Store,
+        current_time: SystemTime,
+    ) {
+        let mut join_handle = self.inner.automatic_media_cleanup_join_handle.lock();
+
+        if join_handle.as_ref().is_some_and(|join_handle| !join_handle.is_finished()) {
+            // There is an ongoing automatic media cache cleanup.
+            return;
+        }
+
+        let policy = self.media_retention_policy();
+        if policy.cleanup_frequency.is_none() || !policy.has_limitations() {
+            // Automatic cleanups are disabled or have no effect.
+            return;
+        }
+
+        let last_media_cleanup_time = *self.inner.last_media_cleanup_time.lock();
+        if last_media_cleanup_time.is_some_and(|last_cleanup_time| {
+            !policy.should_clean_up(current_time, last_cleanup_time)
+        }) {
+            // It is not time to clean up.
+            return;
+        }
+
+        let this = self.clone();
+        let store = store.clone();
+
+        let handle = spawn(async move {
+            if let Err(error) = this.clean_up_media_cache_inner(&store, current_time).await {
+                error!("Failed to run automatic media cache cleanup: {error}");
+            }
+        });
+
+        *join_handle = Some(handle);
     }
 }
 
@@ -238,6 +338,17 @@ where
     }
 }
 
+impl<Time> Drop for MediaServiceInner<Time>
+where
+    Time: TimeProvider,
+{
+    fn drop(&mut self) {
+        if let Some(join_handle) = self.automatic_media_cleanup_join_handle.lock().take() {
+            join_handle.abort();
+        }
+    }
+}
+
 /// An abstract trait that can be used to implement different store backends
 /// for the media cache of the SDK.
 ///
@@ -249,7 +360,7 @@ where
 #[cfg_attr(not(target_arch = "wasm32"), async_trait)]
 pub trait EventCacheStoreMedia: AsyncTraitDeps + Clone {
     /// The error type used by this media cache store.
-    type Error: fmt::Debug + Into<EventCacheStoreError>;
+    type Error: fmt::Debug + fmt::Display + Into<EventCacheStoreError>;
 
     /// The persisted media retention policy in the media cache.
     async fn media_retention_policy_inner(
@@ -401,7 +512,7 @@ impl IgnoreMediaRetentionPolicy {
 
 /// An abstract trait to provide the current `SystemTime` for the
 /// [`MediaService`].
-pub trait TimeProvider {
+pub trait TimeProvider: SendOutsideWasm + SyncOutsideWasm {
     /// The current time.
     fn now(&self) -> SystemTime;
 }
@@ -681,7 +792,7 @@ mod tests {
 
         // By default an empty policy is used.
         assert!(!service.media_retention_policy().has_limitations());
-        service.restore(None);
+        service.restore(None, None);
         assert!(!service.media_retention_policy().has_limitations());
         assert!(!store.accessed());
 
@@ -770,7 +881,7 @@ mod tests {
         let service = MediaService::with_time_provider(MockTimeProvider::new(now));
 
         // Check that restoring the policy works.
-        service.restore(Some(MediaRetentionPolicy::default()));
+        service.restore(Some(MediaRetentionPolicy::default()), None);
         assert_eq!(service.media_retention_policy(), MediaRetentionPolicy::default());
         assert!(!store.accessed());
 
@@ -904,4 +1015,91 @@ mod tests {
         assert!(store.accessed());
         assert_eq!(store.last_media_cleanup_time_inner().await.unwrap(), Some(now));
     }
+
+    #[async_test]
+    async fn test_media_service_automatic_cleanup() {
+        // 64 bytes content.
+        let content = vec![0; 64];
+
+        let uri_1 = mxc_uri!("mxc://localhost/media-1");
+        let request_1 = MediaRequestParameters {
+            source: MediaSource::Plain(uri_1.to_owned()),
+            format: MediaFormat::File,
+        };
+        let uri_2 = mxc_uri!("mxc://localhost/media-2");
+        let request_2 = MediaRequestParameters {
+            source: MediaSource::Plain(uri_2.to_owned()),
+            format: MediaFormat::File,
+        };
+
+        let now = SystemTime::UNIX_EPOCH;
+
+        let store = MockEventCacheStoreMedia::default();
+        let service = MediaService::with_time_provider(MockTimeProvider::new(now));
+
+        // Set an empty policy.
+        let policy = MediaRetentionPolicy::empty();
+        service.set_media_retention_policy(&store, policy).await.unwrap();
+
+        // Add the contents.
+        service
+            .add_media_content(&store, &request_1, content.clone(), IgnoreMediaRetentionPolicy::No)
+            .await
+            .unwrap();
+        service
+            .add_media_content(&store, &request_2, content, IgnoreMediaRetentionPolicy::No)
+            .await
+            .unwrap();
+        assert!(service.inner.automatic_media_cleanup_join_handle.lock().is_none());
+
+        // Try to launch an automatic cleanup.
+        let now = now + Duration::from_secs(60);
+        service.inner.time_provider.set_now(now);
+        service.maybe_spawn_automatic_media_cache_cleanup(&store, now);
+
+        // No cleanup was spawned since automatic cleanups are disabled.
+        assert!(service.inner.automatic_media_cleanup_join_handle.lock().is_none());
+
+        // Set a policy with automatic cleanup every hour.
+        let policy = MediaRetentionPolicy::empty()
+            .with_cleanup_frequency(Some(Duration::from_secs(60 * 60)));
+        let now = now + Duration::from_secs(60);
+        service.inner.time_provider.set_now(now);
+        service.set_media_retention_policy(&store, policy).await.unwrap();
+
+        // No cleanup was spawned since the policy has no limitations.
+        assert!(service.inner.automatic_media_cleanup_join_handle.lock().is_none());
+
+        // Set a policy with automatic cleanup every hour and a max file size.
+        let policy = MediaRetentionPolicy::empty()
+            .with_cleanup_frequency(Some(Duration::from_secs(60 * 60)))
+            .with_max_file_size(Some(512));
+        let now = now + Duration::from_secs(60);
+        service.inner.time_provider.set_now(now);
+        service.set_media_retention_policy(&store, policy).await.unwrap();
+
+        // A cleanup was spawned since there was no last_media_cleanup_time.
+        let join_handle = service.inner.automatic_media_cleanup_join_handle.lock().take().unwrap();
+        join_handle.await.unwrap();
+
+        assert_eq!(store.last_media_cleanup_time_inner().await.unwrap(), Some(now));
+
+        // Try again one minute in the future, nothing is spawned because we need to
+        // wait for one hour.
+        let now = now + Duration::from_secs(60);
+        service.inner.time_provider.set_now(now);
+        service.get_media_content(&store, &request_1).await.unwrap();
+
+        assert!(service.inner.automatic_media_cleanup_join_handle.lock().is_none());
+
+        // Try again 2 hours in the future, another cleanup is spawned.
+        let now = now + Duration::from_secs(2 * 60 * 60);
+        service.inner.time_provider.set_now(now);
+        service.get_media_content_for_uri(&store, uri_1).await.unwrap();
+
+        let join_handle = service.inner.automatic_media_cleanup_join_handle.lock().take().unwrap();
+        join_handle.await.unwrap();
+
+        assert_eq!(store.last_media_cleanup_time_inner().await.unwrap(), Some(now));
+    }
 }
diff --git a/crates/matrix-sdk-base/src/event_cache/store/memory_store.rs b/crates/matrix-sdk-base/src/event_cache/store/memory_store.rs
index 3c211a1ee..69dce88a7 100644
--- a/crates/matrix-sdk-base/src/event_cache/store/memory_store.rs
+++ b/crates/matrix-sdk-base/src/event_cache/store/memory_store.rs
@@ -80,17 +80,20 @@ const NUMBER_OF_MEDIAS: NonZeroUsize = unsafe { NonZeroUsize::new_unchecked(20)
 
 impl Default for MemoryStore {
     fn default() -> Self {
+        // Given that the store is empty, we won't need to clean it up right away.
+        let last_media_cleanup_time = SystemTime::now();
+        let media_service = MediaService::new();
+        media_service.restore(None, Some(last_media_cleanup_time));
+
         Self {
             inner: Arc::new(StdRwLock::new(MemoryStoreInner {
                 media: RingBuffer::new(NUMBER_OF_MEDIAS),
                 leases: Default::default(),
                 events: RelationalLinkedChunk::new(),
                 media_retention_policy: None,
-                // Given that the store is empty, we won't need to clean it up right away.
-                last_media_cleanup_time: SystemTime::now(),
+                last_media_cleanup_time,
             })),
-            // No need to call `restore()` since nothing is persisted.
-            media_service: MediaService::new(),
+            media_service,
         }
     }
 }
diff --git a/crates/matrix-sdk-sqlite/src/event_cache_store.rs b/crates/matrix-sdk-sqlite/src/event_cache_store.rs
index f4b918b64..2ea9f8232 100644
--- a/crates/matrix-sdk-sqlite/src/event_cache_store.rs
+++ b/crates/matrix-sdk-sqlite/src/event_cache_store.rs
@@ -117,7 +117,8 @@ impl SqliteEventCacheStore {
 
         let media_service = MediaService::new();
         let media_retention_policy = conn.get_serialized_kv(keys::MEDIA_RETENTION_POLICY).await?;
-        media_service.restore(media_retention_policy);
+        let last_media_cleanup_time = conn.get_serialized_kv(keys::LAST_MEDIA_CLEANUP_TIME).await?;
+        media_service.restore(media_retention_policy, last_media_cleanup_time);
 
         Ok(Self { store_cipher, pool, media_service })
     }