diff --git a/beacon_node/beacon_chain/src/beacon_chain.rs b/beacon_node/beacon_chain/src/beacon_chain.rs
index 9d204ac7f2..703ed24420 100644
--- a/beacon_node/beacon_chain/src/beacon_chain.rs
+++ b/beacon_node/beacon_chain/src/beacon_chain.rs
@@ -662,7 +662,18 @@ impl<T: BeaconChainTypes> BeaconChain<T> {
             .custody_context()
             .as_ref()
             .into();
-        debug!(?custody_context, "Persisting custody context to store");
+
+        // Pattern match to avoid accidentally missing fields and to ignore deprecated fields.
+        let CustodyContextSsz {
+            validator_custody_at_head,
+            epoch_validator_custody_requirements,
+            persisted_is_supernode: _,
+        } = &custody_context;
+        debug!(
+            validator_custody_at_head,
+            ?epoch_validator_custody_requirements,
+            "Persisting custody context to store"
+        );
 
         persist_custody_context::<T::EthSpec, T::HotStore, T::ColdStore>(
             self.store.clone(),
diff --git a/beacon_node/beacon_chain/src/builder.rs b/beacon_node/beacon_chain/src/builder.rs
index 2c1dae9215..66a54d46e8 100644
--- a/beacon_node/beacon_chain/src/builder.rs
+++ b/beacon_node/beacon_chain/src/builder.rs
@@ -1083,6 +1083,11 @@ where
             let cgc_change_effective_slot =
                 cgc_changed.effective_epoch.start_slot(E::slots_per_epoch());
             beacon_chain.update_data_column_custody_info(Some(cgc_change_effective_slot));
+
+            // Persist change to disk.
+            beacon_chain
+                .persist_custody_context()
+                .map_err(|e| format!("Failed writing updated CGC: {e:?}"))?;
         }
 
         info!(
diff --git a/beacon_node/http_api/src/validator/mod.rs b/beacon_node/http_api/src/validator/mod.rs
index df237d9f9b..a9082df715 100644
--- a/beacon_node/http_api/src/validator/mod.rs
+++ b/beacon_node/http_api/src/validator/mod.rs
@@ -727,6 +727,18 @@ pub fn post_validator_prepare_beacon_proposer<T: BeaconChainTypes>(
                                 debug!(error = %e, "Could not send message to the network service. \
                                 Likely shutdown")
                             });
+
+                            // Write the updated custody context to disk. This happens at most 128
+                            // times ever, so the I/O burden should be extremely minimal. Without a
+                            // write here we risk forgetting custody backfill progress upon an
+                            // unclean shutdown. The custody context is otherwise only persisted in
+                            // `BeaconChain::drop`.
+                            if let Err(error) = chain.persist_custody_context() {
+                                error!(
+                                    ?error,
+                                    "Failed to persist custody context after CGC update"
+                                );
+                            }
                         }
                     }