diff --git a/src/compute-client/src/controller/instance.rs b/src/compute-client/src/controller/instance.rs
index d5a436cb56a29..b74a8fab13023 100644
--- a/src/compute-client/src/controller/instance.rs
+++ b/src/compute-client/src/controller/instance.rs
@@ -1066,7 +1066,9 @@ where
             self.replica_tx.clone(),
         );
 
-        // Take this opportunity to clean up the history we should present.
+        // Apply all pending compaction commands and reduce the history to remove dataflows that
+        // have already been dropped and advance others to their most current as-of.
+        self.send_allow_compaction();
         self.history.reduce();
 
         // Replay the commands at the client, creating new dataflow identifiers.
@@ -1723,11 +1725,19 @@ where
                 .expect("frontiers don't regress");
         }
 
-        // Produce `AllowCompaction` command.
-        self.send(ComputeCommand::AllowCompaction {
-            id,
-            frontier: new_since,
-        });
+        // Update the allowed compaction for this collection.
+        // We defer reporting of non-empty compaction frontiers, to reduce churn when read holds
+        // are downgraded multiple times. Empty frontiers we report immediately, to ensure
+        // dataflows are cleaned up as quickly as possible.
+        if new_since.is_empty() {
+            collection.allowed_compaction = None;
+            self.send(ComputeCommand::AllowCompaction {
+                id,
+                frontier: new_since,
+            })
+        } else {
+            collection.allowed_compaction = Some(new_since);
+        }
     }
 
     /// Fulfills a registered peek and cleans up associated state.
@@ -2060,6 +2070,26 @@ where
         }
     }
 
+    /// Send pending `AllowCompaction` commands.
+    ///
+    /// To reduce network traffic and make the command stream less noisy,
+    /// [`Instance::apply_read_hold_change`] doesn't immediately emit an `AllowCompaction` command
+    /// when a read frontier changes, but instead stashes the new frontier. If another read
+    /// frontier downgrade occurs before the next call to this method, it overrides the previous
+    /// read frontier and only one `AllowCompaction` commands needs to be sent, instead of two.
+    fn send_allow_compaction(&mut self) {
+        let mut commands = Vec::with_capacity(self.collections.len());
+        for (&id, collection) in &mut self.collections {
+            if let Some(frontier) = collection.allowed_compaction.take() {
+                commands.push(ComputeCommand::AllowCompaction { id, frontier });
+            }
+        }
+
+        for command in commands {
+            self.send(command);
+        }
+    }
+
     /// Process pending maintenance work.
     ///
     /// This method is invoked periodically by the global controller.
@@ -2069,6 +2099,7 @@ where
     pub fn maintain(&mut self) {
         self.rehydrate_failed_replicas();
         self.downgrade_warmup_capabilities();
+        self.send_allow_compaction();
         self.schedule_collections();
         self.cleanup_collections();
         self.update_frontier_introspection();
@@ -2131,6 +2162,8 @@ struct CollectionState<T: ComputeControllerTimestamp> {
 
     /// Introspection state associated with this collection.
     introspection: CollectionIntrospection<T>,
+    /// Allowed compaction that has yet to be communicated to replicas.
+    allowed_compaction: Option<Antichain<T>>,
 }
 
 impl<T: ComputeControllerTimestamp> CollectionState<T> {
@@ -2176,6 +2209,7 @@ impl<T: ComputeControllerTimestamp> CollectionState<T> {
             storage_dependencies,
             compute_dependencies,
             introspection,
+            allowed_compaction: None,
         }
     }