diff --git a/beacon_node/beacon_chain/src/data_availability_checker/overflow_lru_cache.rs b/beacon_node/beacon_chain/src/data_availability_checker/overflow_lru_cache.rs
index e2eef45d250..6033293b825 100644
--- a/beacon_node/beacon_chain/src/data_availability_checker/overflow_lru_cache.rs
+++ b/beacon_node/beacon_chain/src/data_availability_checker/overflow_lru_cache.rs
@@ -771,12 +771,13 @@ mod test {
     ) -> Arc<HotColdDB<E, LevelDB<E>, LevelDB<E>>> {
         let hot_path = db_path.path().join("hot_db");
         let cold_path = db_path.path().join("cold_db");
+        let blobs_path = db_path.path().join("blobs_db");
         let config = StoreConfig::default();
 
         HotColdDB::open(
             &hot_path,
             &cold_path,
-            None,
+            &blobs_path,
             |_, _, _| Ok(()),
             config,
             spec,
diff --git a/beacon_node/beacon_chain/tests/op_verification.rs b/beacon_node/beacon_chain/tests/op_verification.rs
index f4af490710d..f6cf40a3962 100644
--- a/beacon_node/beacon_chain/tests/op_verification.rs
+++ b/beacon_node/beacon_chain/tests/op_verification.rs
@@ -29,12 +29,13 @@ fn get_store(db_path: &TempDir) -> Arc<HotColdDB> {
     let spec = test_spec::<E>();
     let hot_path = db_path.path().join("hot_db");
     let cold_path = db_path.path().join("cold_db");
+    let blobs_path = db_path.path().join("blobs_db");
     let config = StoreConfig::default();
     let log = NullLoggerBuilder.build().expect("logger should build");
     HotColdDB::open(
         &hot_path,
         &cold_path,
-        None,
+        &blobs_path,
         |_, _, _| Ok(()),
         config,
         spec,
diff --git a/beacon_node/beacon_chain/tests/store_tests.rs b/beacon_node/beacon_chain/tests/store_tests.rs
index d3f6428851f..c5866ae1e05 100644
--- a/beacon_node/beacon_chain/tests/store_tests.rs
+++ b/beacon_node/beacon_chain/tests/store_tests.rs
@@ -31,7 +31,7 @@ use store::{
     chunked_vector::{chunk_key, Field},
     get_key_for_col,
     iter::{BlockRootsIterator, StateRootsIterator},
-    DBColumn, HotColdDB, KeyValueStore, KeyValueStoreOp, LevelDB, StoreConfig,
+    BlobInfo, DBColumn, HotColdDB, KeyValueStore, KeyValueStoreOp, LevelDB, StoreConfig,
 };
 use tempfile::{tempdir, TempDir};
 use tokio::time::sleep;
@@ -62,12 +62,13 @@ fn get_store_generic(
 ) -> Arc<HotColdDB<E, LevelDB<E>, LevelDB<E>>> {
     let hot_path = db_path.path().join("hot_db");
     let cold_path = db_path.path().join("cold_db");
+    let blobs_path = db_path.path().join("blobs_db");
     let log = test_logger();
 
     HotColdDB::open(
         &hot_path,
         &cold_path,
-        None,
+        &blobs_path,
         |_, _, _| Ok(()),
         config,
         spec,
@@ -3278,6 +3279,40 @@ async fn deneb_prune_blobs_margin_test(margin: u64) {
     check_blob_existence(&harness, oldest_blob_slot, harness.head_slot(), true);
 }
 
+/// Check that a database with `blobs_db=false` can be upgraded to `blobs_db=true` before Deneb.
+#[tokio::test]
+async fn change_to_separate_blobs_db_before_deneb() {
+    let db_path = tempdir().unwrap();
+    let store = get_store(&db_path);
+
+    // Only run this test on forks prior to Deneb. If the blobs database already has blobs, we can't
+    // move it.
+    if store.get_chain_spec().deneb_fork_epoch.is_some() {
+        return;
+    }
+
+    let init_blob_info = store.get_blob_info();
+    assert!(
+        init_blob_info.blobs_db,
+        "separate blobs DB should be the default"
+    );
+
+    // Change to `blobs_db=false` to emulate legacy Deneb DB.
+    let legacy_blob_info = BlobInfo {
+        blobs_db: false,
+        ..init_blob_info
+    };
+    store
+        .compare_and_set_blob_info_with_write(init_blob_info.clone(), legacy_blob_info.clone())
+        .unwrap();
+    assert_eq!(store.get_blob_info(), legacy_blob_info);
+
+    // Re-open the DB and check that `blobs_db` gets changed back to true.
+    drop(store);
+    let store = get_store(&db_path);
+    assert_eq!(store.get_blob_info(), init_blob_info);
+}
+
 /// Check that there are blob sidecars (or not) at every slot in the range.
 fn check_blob_existence(
     harness: &TestHarness,
diff --git a/beacon_node/client/src/builder.rs b/beacon_node/client/src/builder.rs
index fe8a56084d8..cedf347b9a8 100644
--- a/beacon_node/client/src/builder.rs
+++ b/beacon_node/client/src/builder.rs
@@ -901,7 +901,7 @@ where
         mut self,
         hot_path: &Path,
         cold_path: &Path,
-        blobs_path: Option<PathBuf>,
+        blobs_path: &Path,
         config: StoreConfig,
         log: Logger,
     ) -> Result<Self, String> {
diff --git a/beacon_node/client/src/config.rs b/beacon_node/client/src/config.rs
index 492431cd36a..20afdb948bb 100644
--- a/beacon_node/client/src/config.rs
+++ b/beacon_node/client/src/config.rs
@@ -10,8 +10,11 @@ use std::fs;
 use std::path::PathBuf;
 use std::time::Duration;
 use types::Graffiti;
+
 /// Default directory name for the freezer database under the top-level data dir.
 const DEFAULT_FREEZER_DB_DIR: &str = "freezer_db";
+/// Default directory name for the blobs database under the top-level data dir.
+const DEFAULT_BLOBS_DB_DIR: &str = "blobs_db";
 
 /// Defines how the client should initialize the `BeaconChain` and other components.
 #[derive(Debug, Clone, Serialize, Deserialize, Default)]
@@ -146,12 +149,19 @@ impl Config {
             .unwrap_or_else(|| self.default_freezer_db_path())
     }
 
+    /// Fetch default path to use for the blobs database.
+    fn default_blobs_db_path(&self) -> PathBuf {
+        self.get_data_dir().join(DEFAULT_BLOBS_DB_DIR)
+    }
+
     /// Returns the path to which the client may initialize the on-disk blobs database.
     ///
     /// Will attempt to use the user-supplied path from e.g. the CLI, or will default
     /// to None.
-    pub fn get_blobs_db_path(&self) -> Option<PathBuf> {
-        self.blobs_db_path.clone()
+    pub fn get_blobs_db_path(&self) -> PathBuf {
+        self.blobs_db_path
+            .clone()
+            .unwrap_or_else(|| self.default_blobs_db_path())
     }
 
     /// Get the freezer DB path, creating it if necessary.
@@ -160,11 +170,8 @@ impl Config {
     }
 
     /// Get the blobs DB path, creating it if necessary.
-    pub fn create_blobs_db_path(&self) -> Result<Option<PathBuf>, String> {
-        match self.get_blobs_db_path() {
-            Some(blobs_db_path) => Ok(Some(ensure_dir_exists(blobs_db_path)?)),
-            None => Ok(None),
-        }
+    pub fn create_blobs_db_path(&self) -> Result<PathBuf, String> {
+        ensure_dir_exists(self.get_blobs_db_path())
     }
 
     /// Returns the "modern" path to the data_dir.
diff --git a/beacon_node/src/lib.rs b/beacon_node/src/lib.rs
index 085a2a78241..cf6d627c304 100644
--- a/beacon_node/src/lib.rs
+++ b/beacon_node/src/lib.rs
@@ -89,7 +89,7 @@ impl<E: EthSpec> ProductionBeaconNode<E> {
             .disk_store(
                 &db_path,
                 &freezer_db_path,
-                blobs_db_path,
+                &blobs_db_path,
                 store_config,
                 log.clone(),
             )?;
diff --git a/beacon_node/store/src/hot_cold_store.rs b/beacon_node/store/src/hot_cold_store.rs
index 6e2a2ae583e..43e14c30970 100644
--- a/beacon_node/store/src/hot_cold_store.rs
+++ b/beacon_node/store/src/hot_cold_store.rs
@@ -35,7 +35,7 @@ use state_processing::{
 use std::cmp::min;
 use std::convert::TryInto;
 use std::marker::PhantomData;
-use std::path::{Path, PathBuf};
+use std::path::Path;
 use std::sync::Arc;
 use std::time::Duration;
 use types::blob_sidecar::BlobSidecarList;
@@ -61,7 +61,7 @@ pub struct HotColdDB<E: EthSpec, Hot: ItemStore<E>, Cold: ItemStore<E>> {
     /// Cold database containing compact historical data.
     pub cold_db: Cold,
     /// Database containing blobs. If None, store falls back to use `cold_db`.
-    pub blobs_db: Option<Cold>,
+    pub blobs_db: Cold,
     /// Hot database containing duplicated but quick-to-access recent data.
     ///
     /// The hot database also contains all blocks.
@@ -138,7 +138,6 @@ pub enum HotColdDBError {
     MissingExecutionPayload(Hash256),
     MissingFullBlockExecutionPayloadPruned(Hash256, Slot),
     MissingAnchorInfo,
-    MissingPathToBlobsDatabase,
     BlobsPreviouslyInDefaultStore,
     HotStateSummaryError(BeaconStateError),
     RestorePointDecodeError(ssz::DecodeError),
@@ -178,7 +177,7 @@ impl<E: EthSpec> HotColdDB<E, MemoryStore<E>, MemoryStore<E>> {
             anchor_info: RwLock::new(None),
             blob_info: RwLock::new(BlobInfo::default()),
             cold_db: MemoryStore::open(),
-            blobs_db: Some(MemoryStore::open()),
+            blobs_db: MemoryStore::open(),
             hot_db: MemoryStore::open(),
             block_cache: Mutex::new(BlockCache::new(config.block_cache_size)),
             state_cache: Mutex::new(LruCache::new(config.historic_state_cache_size)),
@@ -202,7 +201,7 @@ impl<E: EthSpec> HotColdDB<E, LevelDB<E>, LevelDB<E>> {
     pub fn open(
         hot_path: &Path,
         cold_path: &Path,
-        blobs_db_path: Option<PathBuf>,
+        blobs_db_path: &Path,
         migrate_schema: impl FnOnce(Arc<Self>, SchemaVersion, SchemaVersion) -> Result<(), Error>,
         config: StoreConfig,
         spec: ChainSpec,
@@ -215,7 +214,7 @@ impl<E: EthSpec> HotColdDB<E, LevelDB<E>, LevelDB<E>> {
             anchor_info: RwLock::new(None),
             blob_info: RwLock::new(BlobInfo::default()),
             cold_db: LevelDB::open(cold_path)?,
-            blobs_db: None,
+            blobs_db: LevelDB::open(blobs_db_path)?,
             hot_db: LevelDB::open(hot_path)?,
             block_cache: Mutex::new(BlockCache::new(config.block_cache_size)),
             state_cache: Mutex::new(LruCache::new(config.historic_state_cache_size)),
@@ -271,37 +270,29 @@ impl<E: EthSpec> HotColdDB<E, LevelDB<E>, LevelDB<E>> {
             Some(blob_info) => {
                 // If the oldest block slot is already set do not allow the blob DB path to be
                 // changed (require manual migration).
-                if blob_info.oldest_blob_slot.is_some() {
-                    if blobs_db_path.is_some() && !blob_info.blobs_db {
-                        return Err(HotColdDBError::BlobsPreviouslyInDefaultStore.into());
-                    } else if blobs_db_path.is_none() && blob_info.blobs_db {
-                        return Err(HotColdDBError::MissingPathToBlobsDatabase.into());
-                    }
+                if blob_info.oldest_blob_slot.is_some() && !blob_info.blobs_db {
+                    return Err(HotColdDBError::BlobsPreviouslyInDefaultStore.into());
                 }
                 // Set the oldest blob slot to the Deneb fork slot if it is not yet set.
+                // Always initialize `blobs_db` to true, we no longer support storing the blobs
+                // in the freezer DB, because the UX is strictly worse for relocating the DB.
                 let oldest_blob_slot = blob_info.oldest_blob_slot.or(deneb_fork_slot);
                 BlobInfo {
                     oldest_blob_slot,
-                    blobs_db: blobs_db_path.is_some(),
+                    blobs_db: true,
                 }
             }
             // First start.
             None => BlobInfo {
                 // Set the oldest blob slot to the Deneb fork slot if it is not yet set.
                 oldest_blob_slot: deneb_fork_slot,
-                blobs_db: blobs_db_path.is_some(),
+                blobs_db: true,
             },
         };
-        if new_blob_info.blobs_db {
-            if let Some(path) = &blobs_db_path {
-                db.blobs_db = Some(LevelDB::open(path.as_path())?);
-            }
-        }
         db.compare_and_set_blob_info_with_write(<_>::default(), new_blob_info.clone())?;
         info!(
             db.log,
             "Blob DB initialized";
-            "separate_db" => new_blob_info.blobs_db,
             "path" => ?blobs_db_path,
             "oldest_blob_slot" => ?new_blob_info.oldest_blob_slot,
         );
@@ -575,8 +566,8 @@ impl<E: EthSpec, Hot: ItemStore<E>, Cold: ItemStore<E>> HotColdDB<E, Hot, Cold>
 
     /// Check if the blobs for a block exists on disk.
     pub fn blobs_exist(&self, block_root: &Hash256) -> Result<bool, Error> {
-        let blobs_db = self.blobs_db.as_ref().unwrap_or(&self.cold_db);
-        blobs_db.key_exists(DBColumn::BeaconBlob.into(), block_root.as_bytes())
+        self.blobs_db
+            .key_exists(DBColumn::BeaconBlob.into(), block_root.as_bytes())
     }
 
     /// Determine whether a block exists in the database.
@@ -592,13 +583,12 @@ impl<E: EthSpec, Hot: ItemStore<E>, Cold: ItemStore<E>> HotColdDB<E, Hot, Cold>
             .key_delete(DBColumn::BeaconBlock.into(), block_root.as_bytes())?;
         self.hot_db
             .key_delete(DBColumn::ExecPayload.into(), block_root.as_bytes())?;
-        let blobs_db = self.blobs_db.as_ref().unwrap_or(&self.cold_db);
-        blobs_db.key_delete(DBColumn::BeaconBlob.into(), block_root.as_bytes())
+        self.blobs_db
+            .key_delete(DBColumn::BeaconBlob.into(), block_root.as_bytes())
     }
 
     pub fn put_blobs(&self, block_root: &Hash256, blobs: BlobSidecarList<E>) -> Result<(), Error> {
-        let blobs_db = self.blobs_db.as_ref().unwrap_or(&self.cold_db);
-        blobs_db.put_bytes(
+        self.blobs_db.put_bytes(
             DBColumn::BeaconBlob.into(),
             block_root.as_bytes(),
             &blobs.as_ssz_bytes(),
@@ -988,9 +978,9 @@ impl<E: EthSpec, Hot: ItemStore<E>, Cold: ItemStore<E>> HotColdDB<E, Hot, Cold>
         let mut guard = self.block_cache.lock();
 
         let blob_cache_ops = blobs_ops.clone();
-        let blobs_db = self.blobs_db.as_ref().unwrap_or(&self.cold_db);
         // Try to execute blobs store ops.
-        blobs_db.do_atomically(self.convert_to_kv_batch(blobs_ops)?)?;
+        self.blobs_db
+            .do_atomically(self.convert_to_kv_batch(blobs_ops)?)?;
 
         let hot_db_cache_ops = hot_db_ops.clone();
         // Try to execute hot db store ops.
@@ -1018,7 +1008,8 @@ impl<E: EthSpec, Hot: ItemStore<E>, Cold: ItemStore<E>> HotColdDB<E, Hot, Cold>
                 };
                 *op = reverse_op;
             }
-            blobs_db.do_atomically(self.convert_to_kv_batch(blob_cache_ops)?)?;
+            self.blobs_db
+                .do_atomically(self.convert_to_kv_batch(blob_cache_ops)?)?;
             return Err(e);
         }
 
@@ -1436,15 +1427,16 @@ impl<E: EthSpec, Hot: ItemStore<E>, Cold: ItemStore<E>> HotColdDB<E, Hot, Cold>
 
     /// Fetch blobs for a given block from the store.
     pub fn get_blobs(&self, block_root: &Hash256) -> Result<Option<BlobSidecarList<E>>, Error> {
-        let blobs_db = self.blobs_db.as_ref().unwrap_or(&self.cold_db);
-
         // Check the cache.
         if let Some(blobs) = self.block_cache.lock().get_blobs(block_root) {
             metrics::inc_counter(&metrics::BEACON_BLOBS_CACHE_HIT_COUNT);
             return Ok(Some(blobs.clone()));
         }
 
-        match blobs_db.get_bytes(DBColumn::BeaconBlob.into(), block_root.as_bytes())? {
+        match self
+            .blobs_db
+            .get_bytes(DBColumn::BeaconBlob.into(), block_root.as_bytes())?
+        {
             Some(ref blobs_bytes) => {
                 let blobs = BlobSidecarList::from_ssz_bytes(blobs_bytes)?;
                 self.block_cache
@@ -1640,7 +1632,7 @@ impl<E: EthSpec, Hot: ItemStore<E>, Cold: ItemStore<E>> HotColdDB<E, Hot, Cold>
         });
         let blob_info = BlobInfo {
             oldest_blob_slot,
-            blobs_db: self.blobs_db.is_some(),
+            blobs_db: true,
         };
         self.compare_and_set_blob_info(self.get_blob_info(), blob_info)
     }
diff --git a/beacon_node/store/src/metadata.rs b/beacon_node/store/src/metadata.rs
index 124c9a2f586..6fef74d7ff0 100644
--- a/beacon_node/store/src/metadata.rs
+++ b/beacon_node/store/src/metadata.rs
@@ -135,7 +135,7 @@ pub struct BlobInfo {
     /// If the `oldest_blob_slot` is `None` then this means that the Deneb fork epoch is not yet
     /// known.
     pub oldest_blob_slot: Option<Slot>,
-    /// A separate blobs database is in use.
+    /// A separate blobs database is in use (deprecated, always `true`).
     pub blobs_db: bool,
 }
 
diff --git a/database_manager/src/lib.rs b/database_manager/src/lib.rs
index 93654b8dd50..95af4d63821 100644
--- a/database_manager/src/lib.rs
+++ b/database_manager/src/lib.rs
@@ -210,7 +210,7 @@ pub fn display_db_version<E: EthSpec>(
     HotColdDB::<E, LevelDB<E>, LevelDB<E>>::open(
         &hot_path,
         &cold_path,
-        blobs_path,
+        &blobs_path,
         |_, from, _| {
             version = from;
             Ok(())
@@ -288,7 +288,7 @@ pub fn inspect_db<E: EthSpec>(
     let db = HotColdDB::<E, LevelDB<E>, LevelDB<E>>::open(
         &hot_path,
         &cold_path,
-        blobs_path,
+        &blobs_path,
         |_, _, _| Ok(()),
         client_config.store,
         spec,
@@ -410,7 +410,7 @@ pub fn migrate_db<E: EthSpec>(
     let db = HotColdDB::<E, LevelDB<E>, LevelDB<E>>::open(
         &hot_path,
         &cold_path,
-        blobs_path,
+        &blobs_path,
         |_, db_initial_version, _| {
             from = db_initial_version;
             Ok(())
@@ -450,7 +450,7 @@ pub fn prune_payloads<E: EthSpec>(
     let db = HotColdDB::<E, LevelDB<E>, LevelDB<E>>::open(
         &hot_path,
         &cold_path,
-        blobs_path,
+        &blobs_path,
         |_, _, _| Ok(()),
         client_config.store,
         spec.clone(),
@@ -476,7 +476,7 @@ pub fn prune_blobs<E: EthSpec>(
     let db = HotColdDB::<E, LevelDB<E>, LevelDB<E>>::open(
         &hot_path,
         &cold_path,
-        blobs_path,
+        &blobs_path,
         |_, _, _| Ok(()),
         client_config.store,
         spec.clone(),
@@ -512,7 +512,7 @@ pub fn prune_states<E: EthSpec>(
     let db = HotColdDB::<E, LevelDB<E>, LevelDB<E>>::open(
         &hot_path,
         &cold_path,
-        blobs_path,
+        &blobs_path,
         |_, _, _| Ok(()),
         client_config.store,
         spec.clone(),