diff --git a/zebra-state/src/config.rs b/zebra-state/src/config.rs
index e84417099e2..555bd2a5c84 100644
--- a/zebra-state/src/config.rs
+++ b/zebra-state/src/config.rs
@@ -1,6 +1,13 @@
-use std::path::PathBuf;
+//! Cached state configuration for Zebra.
+
+use std::{
+    fs::{canonicalize, remove_dir_all, DirEntry, ReadDir},
+    path::{Path, PathBuf},
+};
 
 use serde::{Deserialize, Serialize};
+use tokio::task::{spawn_blocking, JoinHandle};
+use tracing::Span;
 
 use zebra_chain::parameters::Network;
 
@@ -57,6 +64,13 @@ pub struct Config {
     ///
     /// Set to `None` by default: Zebra continues syncing indefinitely.
     pub debug_stop_at_height: Option<u32>,
+
+    /// Whether to delete the old database directories when present.
+    ///
+    /// Set to `true` by default. If this is set to `false`,
+    /// no check for old database versions will be made and nothing will be
+    /// deleted.
+    pub delete_old_database: bool,
 }
 
 fn gen_temp_path(prefix: &str) -> PathBuf {
@@ -108,6 +122,125 @@ impl Default for Config {
             cache_dir,
             ephemeral: false,
             debug_stop_at_height: None,
+            delete_old_database: true,
+        }
+    }
+}
+
+// Cleaning up old database versions
+
+/// Spawns a task that checks if there are old database folders,
+/// and deletes them from the filesystem.
+///
+/// Iterate over the files and directories in the databases folder and delete if:
+/// - The state directory exists.
+/// - The entry is a directory.
+/// - The directory name has a prefix `v`.
+/// - The directory name without the prefix can be parsed as an unsigned number.
+/// - The parsed number is lower than the hardcoded `DATABASE_FORMAT_VERSION`.
+pub fn check_and_delete_old_databases(config: Config) -> JoinHandle<()> {
+    let current_span = Span::current();
+
+    spawn_blocking(move || {
+        current_span.in_scope(|| {
+            delete_old_databases(config);
+            info!("finished old database version cleanup task");
+        })
+    })
+}
+
+/// Check if there are old database folders and delete them from the filesystem.
+///
+/// See [`check_and_delete_old_databases`] for details.
+fn delete_old_databases(config: Config) {
+    if config.ephemeral || !config.delete_old_database {
+        return;
+    }
+
+    info!("checking for old database versions");
+
+    let state_dir = config.cache_dir.join("state");
+    if let Some(state_dir) = read_dir(&state_dir) {
+        for entry in state_dir.flatten() {
+            let deleted_state = check_and_delete_database(&config, &entry);
+
+            if let Some(deleted_state) = deleted_state {
+                info!(?deleted_state, "deleted outdated state directory");
+            }
         }
     }
 }
+
+/// Return a `ReadDir` for `dir`, after checking that `dir` exists and can be read.
+///
+/// Returns `None` if any operation fails.
+fn read_dir(dir: &Path) -> Option<ReadDir> {
+    if dir.exists() {
+        if let Ok(read_dir) = dir.read_dir() {
+            return Some(read_dir);
+        }
+    }
+    None
+}
+
+/// Check if `entry` is an old database directory, and delete it from the filesystem.
+/// See [`check_and_delete_old_databases`] for details.
+///
+/// If the directory was deleted, returns its path.
+fn check_and_delete_database(config: &Config, entry: &DirEntry) -> Option<PathBuf> {
+    let dir_name = parse_dir_name(entry)?;
+    let version_number = parse_version_number(&dir_name)?;
+
+    if version_number >= crate::constants::DATABASE_FORMAT_VERSION {
+        return None;
+    }
+
+    let outdated_path = entry.path();
+
+    // # Correctness
+    //
+    // Check that the path we're about to delete is inside the cache directory.
+    // If the user has symlinked the outdated state directory to a non-cache directory,
+    // we don't want to delete it, because it might contain other files.
+    //
+    // We don't attempt to guard against malicious symlinks created by attackers
+    // (TOCTOU attacks). Zebra should not be run with elevated privileges.
+    let cache_path = canonicalize(&config.cache_dir).ok()?;
+    let outdated_path = canonicalize(outdated_path).ok()?;
+
+    if !outdated_path.starts_with(&cache_path) {
+        info!(
+            skipped_path = ?outdated_path,
+            ?cache_path,
+            "skipped cleanup of outdated state directory: state is outside cache directory",
+        );
+
+        return None;
+    }
+
+    remove_dir_all(&outdated_path).ok().map(|()| outdated_path)
+}
+
+/// Check if `entry` is a directory with a valid UTF-8 name.
+/// (State directory names are guaranteed to be UTF-8.)
+///
+/// Returns `None` if any operation fails.
+fn parse_dir_name(entry: &DirEntry) -> Option<String> {
+    if let Ok(file_type) = entry.file_type() {
+        if file_type.is_dir() {
+            if let Ok(dir_name) = entry.file_name().into_string() {
+                return Some(dir_name);
+            }
+        }
+    }
+    None
+}
+
+/// Parse the state version number from `dir_name`.
+///
+/// Returns `None` if parsing fails, or the directory name is not in the expected format.
+fn parse_version_number(dir_name: &str) -> Option<u32> {
+    dir_name
+        .strip_prefix('v')
+        .and_then(|version| version.parse().ok())
+}
diff --git a/zebra-state/src/lib.rs b/zebra-state/src/lib.rs
index 3e8601bd934..86d87d9aeda 100644
--- a/zebra-state/src/lib.rs
+++ b/zebra-state/src/lib.rs
@@ -28,7 +28,7 @@ mod util;
 #[cfg(test)]
 mod tests;
 
-pub use config::Config;
+pub use config::{check_and_delete_old_databases, Config};
 pub use constants::MAX_BLOCK_REORG_HEIGHT;
 pub use error::{BoxError, CloneError, CommitBlockError, ValidateContextError};
 pub use request::{FinalizedBlock, HashOrHeight, PreparedBlock, ReadRequest, Request};
diff --git a/zebrad/src/commands/start.rs b/zebrad/src/commands/start.rs
index 9a1bce4b3b1..ff1d592e6a7 100644
--- a/zebrad/src/commands/start.rs
+++ b/zebrad/src/commands/start.rs
@@ -37,6 +37,8 @@
 //!    * contextually verifies blocks
 //!    * handles in-memory storage of multiple non-finalized chains
 //!    * handles permanent storage of the best finalized chain
+//!  * Old State Version Cleanup Task
+//!    * deletes outdated state versions
 //!  * Block Gossip Task
 //!    * runs in the background and continuously queries the state for
 //!      newly committed blocks to be gossiped to peers
@@ -218,6 +220,9 @@ impl StartCmd {
                 .in_current_span(),
         );
 
+        let mut old_databases_task_handle =
+            zebra_state::check_and_delete_old_databases(config.state.clone());
+
         info!("spawned initial Zebra tasks");
 
         // TODO: put tasks into an ongoing FuturesUnordered and a startup FuturesUnordered?
@@ -235,6 +240,8 @@ impl StartCmd {
         // startup tasks
         let groth16_download_handle_fused = (&mut groth16_download_handle).fuse();
         pin!(groth16_download_handle_fused);
+        let old_databases_task_handle_fused = (&mut old_databases_task_handle).fuse();
+        pin!(old_databases_task_handle_fused);
 
         // Wait for tasks to finish
         let exit_status = loop {
@@ -297,6 +304,16 @@ impl StartCmd {
                     exit_when_task_finishes = false;
                     Ok(())
                 }
+
+                // The same for the old databases task, we expect it to finish while Zebra is running.
+                old_databases_result = &mut old_databases_task_handle_fused => {
+                    old_databases_result
+                        .unwrap_or_else(|_| panic!(
+                            "unexpected panic deleting old database directories"));
+
+                    exit_when_task_finishes = false;
+                    Ok(())
+                }
             };
 
             // Stop Zebra if a task finished and returned an error,
@@ -324,6 +341,7 @@ impl StartCmd {
 
         // startup tasks
         groth16_download_handle.abort();
+        old_databases_task_handle.abort();
 
         exit_status
     }
diff --git a/zebrad/tests/acceptance.rs b/zebrad/tests/acceptance.rs
index e3eaf37ee99..f969febd87e 100644
--- a/zebrad/tests/acceptance.rs
+++ b/zebrad/tests/acceptance.rs
@@ -1642,6 +1642,70 @@ async fn fully_synced_rpc_test() -> Result<()> {
     Ok(())
 }
 
+#[tokio::test]
+async fn delete_old_databases() -> Result<()> {
+    use std::fs::{canonicalize, create_dir};
+
+    zebra_test::init();
+
+    let mut config = default_test_config()?;
+    let run_dir = testdir()?;
+    let cache_dir = run_dir.path().join("state");
+
+    // create cache dir
+    create_dir(cache_dir.clone())?;
+
+    // create a v1 dir outside cache dir that should not be deleted
+    let outside_dir = run_dir.path().join("v1");
+    create_dir(&outside_dir)?;
+    assert!(outside_dir.as_path().exists());
+
+    // create a `v1` dir inside cache dir that should be deleted
+    let inside_dir = cache_dir.join("v1");
+    create_dir(&inside_dir)?;
+    let canonicalized_inside_dir = canonicalize(inside_dir.clone()).ok().unwrap();
+    assert!(inside_dir.as_path().exists());
+
+    // modify config with our cache dir and not ephemeral configuration
+    // (delete old databases function will not run when ephemeral = true)
+    config.state.cache_dir = cache_dir;
+    config.state.ephemeral = false;
+
+    // run zebra with our config
+    let mut child = run_dir
+        .with_config(&mut config)?
+        .spawn_child(args!["start"])?;
+
+    // delete checker running
+    child.expect_stdout_line_matches("checking for old database versions".to_string())?;
+
+    // inside dir was deleted
+    child.expect_stdout_line_matches(format!(
+        "deleted outdated state directory deleted_state={:?}",
+        canonicalized_inside_dir
+    ))?;
+    assert!(!inside_dir.as_path().exists());
+
+    // deleting old databases task ended
+    child.expect_stdout_line_matches("finished old database version cleanup task".to_string())?;
+
+    // outside dir was not deleted
+    assert!(outside_dir.as_path().exists());
+
+    // finish
+    child.kill()?;
+
+    let output = child.wait_with_output()?;
+    let output = output.assert_failure()?;
+
+    // [Note on port conflict](#Note on port conflict)
+    output
+        .assert_was_killed()
+        .wrap_err("Possible port conflict. Are there other acceptance tests running?")?;
+
+    Ok(())
+}
+
 /// Test sending transactions using a lightwalletd instance connected to a zebrad instance.
 ///
 /// See [`common::lightwalletd::send_transaction_test`] for more information.