diff --git a/crates/engine/tree/src/tree/mod.rs b/crates/engine/tree/src/tree/mod.rs
index 25c8010c1f71..4d967cf509ed 100644
--- a/crates/engine/tree/src/tree/mod.rs
+++ b/crates/engine/tree/src/tree/mod.rs
@@ -44,7 +44,10 @@ use reth_trie::HashedPostState;
 use std::{
     collections::{BTreeMap, HashMap, HashSet},
     ops::Bound,
-    sync::{mpsc::Receiver, Arc},
+    sync::{
+        mpsc::{Receiver, RecvError, RecvTimeoutError},
+        Arc,
+    },
     time::Instant,
 };
 use tokio::sync::{
@@ -539,15 +542,54 @@ where
     ///
     /// This will block the current thread and process incoming messages.
     pub fn run(mut self) {
-        while let Ok(msg) = self.incoming.recv() {
-            self.run_once(msg);
+        loop {
+            match self.try_recv_engine_message() {
+                Ok(Some(msg)) => {
+                    self.on_engine_message(msg);
+                }
+                Ok(None) => {
+                    debug!(target: "engine", "received no engine message for some time, while waiting for persistence task to complete");
+                }
+                Err(err) => {
+                    error!(target: "engine", "Engine channel disconnected");
+                    return
+                }
+            }
+
+            self.advance_persistence();
         }
     }
 
-    /// Run the engine API handler once.
-    fn run_once(&mut self, msg: FromEngine<BeaconEngineMessage<T>>) {
-        self.on_engine_message(msg);
+    /// Attempts to receive the next engine request.
+    ///
+    /// If there's currently no persistence action in progress, this will block until a new request
+    /// is received. If there's a persistence action in progress, this will try to receive the
+    /// next request with a timeout to not block indefinitely and return `Ok(None)` if no request is
+    /// received in time.
+    ///
+    /// Returns an error if the engine channel is disconnected.
+    fn try_recv_engine_message(
+        &self,
+    ) -> Result<Option<FromEngine<BeaconEngineMessage<T>>>, RecvError> {
+        if self.persistence_state.in_progress() {
+            // try to receive the next request with a timeout to not block indefinitely
+            match self.incoming.recv_timeout(std::time::Duration::from_millis(500)) {
+                Ok(msg) => Ok(Some(msg)),
+                Err(err) => match err {
+                    RecvTimeoutError::Timeout => Ok(None),
+                    RecvTimeoutError::Disconnected => Err(RecvError),
+                },
+            }
+        } else {
+            self.incoming.recv().map(Some)
+        }
+    }
 
+    /// Attempts to advance the persistence state.
+    ///
+    /// If we're currently awaiting a response this will try to receive the response (non-blocking)
+    /// or send a new persistence action if necessary.
+    fn advance_persistence(&mut self) {
         if self.should_persist() && !self.persistence_state.in_progress() {
             let blocks_to_persist = self.get_canonical_blocks_to_persist();
             if !blocks_to_persist.is_empty() {