diff --git a/Cargo.lock b/Cargo.lock
index 0dd0e763..e06d7ff0 100644
--- a/Cargo.lock
+++ b/Cargo.lock
@@ -1716,6 +1716,7 @@ dependencies = [
  "tokio",
  "tracing",
  "tracing-subscriber",
+ "tracing-test",
  "tree_hash",
  "url",
 ]
@@ -6193,6 +6194,27 @@ dependencies = [
  "tracing-serde",
 ]
 
+[[package]]
+name = "tracing-test"
+version = "0.2.5"
+source = "registry+https://github.com/rust-lang/crates.io-index"
+checksum = "557b891436fe0d5e0e363427fc7f217abf9ccd510d5136549847bdcbcd011d68"
+dependencies = [
+ "tracing-core",
+ "tracing-subscriber",
+ "tracing-test-macro",
+]
+
+[[package]]
+name = "tracing-test-macro"
+version = "0.2.5"
+source = "registry+https://github.com/rust-lang/crates.io-index"
+checksum = "04659ddb06c87d233c566112c1c9c5b9e98256d9af50ec3bc9c8327f873a7568"
+dependencies = [
+ "quote",
+ "syn 2.0.106",
+]
+
 [[package]]
 name = "tree_hash"
 version = "0.9.1"
diff --git a/Cargo.toml b/Cargo.toml
index dc5ee88d..6ea8ba96 100644
--- a/Cargo.toml
+++ b/Cargo.toml
@@ -74,6 +74,7 @@ tower-http = { version = "0.6", features = ["trace"] }
 tracing = "0.1.40"
 tracing-appender = "0.2.3"
 tracing-subscriber = { version = "0.3.18", features = ["env-filter", "json"] }
+tracing-test = { version = "0.2.5", features = ["no-env-filter"] }
 tree_hash = "0.9"
 tree_hash_derive = "0.9"
 typenum = "1.17.0"
diff --git a/config.example.toml b/config.example.toml
index 67085409..5b69f108 100644
--- a/config.example.toml
+++ b/config.example.toml
@@ -165,7 +165,8 @@ port = 20000
 # Number of JWT authentication attempts a client can fail before blocking that client temporarily from Signer access
 # OPTIONAL, DEFAULT: 3
 jwt_auth_fail_limit = 3
-# How long to block a client from Signer access, in seconds, if it failed JWT authentication too many times
+# How long to block a client from Signer access, in seconds, if it failed JWT authentication too many times.
+# This also defines the interval at which failed attempts are regularly checked and expired ones are cleaned up.
 # OPTIONAL, DEFAULT: 300
 jwt_auth_fail_timeout_seconds = 300
 
diff --git a/crates/common/src/config/signer.rs b/crates/common/src/config/signer.rs
index 4e040701..b4c5db16 100644
--- a/crates/common/src/config/signer.rs
+++ b/crates/common/src/config/signer.rs
@@ -88,7 +88,8 @@ pub struct SignerConfig {
     pub jwt_auth_fail_limit: u32,
 
     /// Duration in seconds to rate limit an endpoint after the JWT auth failure
-    /// limit has been reached
+    /// limit has been reached. This also defines the interval at which failed
+    /// attempts are regularly checked and expired ones are cleaned up.
     #[serde(default = "default_u32::<SIGNER_JWT_AUTH_FAIL_TIMEOUT_SECONDS_DEFAULT>")]
     pub jwt_auth_fail_timeout_seconds: u32,
 
diff --git a/crates/signer/src/service.rs b/crates/signer/src/service.rs
index e59ca920..e0dd6de6 100644
--- a/crates/signer/src/service.rs
+++ b/crates/signer/src/service.rs
@@ -143,6 +143,22 @@ impl SigningService {
             .route_layer(middleware::from_fn(log_request))
             .route(STATUS_PATH, get(handle_status));
 
+        // Run the JWT cleaning task
+        let jwt_cleaning_task = tokio::spawn(async move {
+            let mut interval = tokio::time::interval(state.jwt_auth_fail_timeout);
+            loop {
+                interval.tick().await;
+                let mut failures = state.jwt_auth_failures.write().await;
+                let before = failures.len();
+                failures
+                    .retain(|_, info| info.last_failure.elapsed() < state.jwt_auth_fail_timeout);
+                let after = failures.len();
+                if before != after {
+                    debug!("Cleaned up {} old JWT auth failure entries", before - after);
+                }
+            }
+        });
+
         let server_result = if let Some(tls_config) = config.tls_certificates {
             if CryptoProvider::get_default().is_none() {
                 // Install the AWS-LC provider if no default is set, usually for CI
@@ -184,6 +200,10 @@ impl SigningService {
                 )
                 .await
         };
+
+        // Shutdown the JWT cleaning task
+        jwt_cleaning_task.abort();
+
         server_result.wrap_err("signer service exited")
     }
 
diff --git a/tests/Cargo.toml b/tests/Cargo.toml
index 6cd2b829..5b373706 100644
--- a/tests/Cargo.toml
+++ b/tests/Cargo.toml
@@ -21,3 +21,6 @@ tracing.workspace = true
 tracing-subscriber.workspace = true
 tree_hash.workspace = true
 url.workspace = true
+
+[dev-dependencies]
+tracing-test.workspace = true
diff --git a/tests/tests/signer_jwt_auth_cleanup.rs b/tests/tests/signer_jwt_auth_cleanup.rs
new file mode 100644
index 00000000..d6fde2a4
--- /dev/null
+++ b/tests/tests/signer_jwt_auth_cleanup.rs
@@ -0,0 +1,70 @@
+use std::{collections::HashMap, time::Duration};
+
+use alloy::primitives::b256;
+use cb_common::{
+    commit::constants::GET_PUBKEYS_PATH,
+    config::{ModuleSigningConfig, load_module_signing_configs},
+    types::ModuleId,
+    utils::create_jwt,
+};
+use cb_tests::{
+    signer_service::start_server,
+    utils::{self},
+};
+use eyre::Result;
+use reqwest::StatusCode;
+
+const JWT_MODULE: &str = "test-module";
+const JWT_SECRET: &str = "test-jwt-secret";
+const ADMIN_SECRET: &str = "test-admin-secret";
+
+async fn create_mod_signing_configs() -> HashMap<ModuleId, ModuleSigningConfig> {
+    let mut cfg =
+        utils::get_commit_boost_config(utils::get_pbs_static_config(utils::get_pbs_config(0)));
+
+    let module_id = ModuleId(JWT_MODULE.to_string());
+    let signing_id = b256!("0101010101010101010101010101010101010101010101010101010101010101");
+
+    cfg.modules = Some(vec![utils::create_module_config(module_id.clone(), signing_id)]);
+
+    let jwts = HashMap::from([(module_id.clone(), JWT_SECRET.to_string())]);
+
+    load_module_signing_configs(&cfg, &jwts).unwrap()
+}
+
+#[tokio::test]
+#[tracing_test::traced_test]
+async fn test_signer_jwt_fail_cleanup() -> Result<()> {
+    // setup_test_env() isn't used because we want to capture logs with tracing_test
+    let module_id = ModuleId(JWT_MODULE.to_string());
+    let mod_cfgs = create_mod_signing_configs().await;
+    let start_config = start_server(20102, &mod_cfgs, ADMIN_SECRET.to_string(), false).await?;
+    let mod_cfg = mod_cfgs.get(&module_id).expect("JWT config for test module not found");
+
+    // Run as many pubkeys requests as the fail limit
+    let jwt = create_jwt(&module_id, "incorrect secret", GET_PUBKEYS_PATH, None)?;
+    let client = reqwest::Client::new();
+    let url = format!("http://{}{}", start_config.endpoint, GET_PUBKEYS_PATH);
+    for _ in 0..start_config.jwt_auth_fail_limit {
+        let response = client.get(&url).bearer_auth(&jwt).send().await?;
+        assert!(response.status() == StatusCode::UNAUTHORIZED);
+    }
+
+    // Run another request - this should fail due to rate limiting now
+    let jwt = create_jwt(&module_id, &mod_cfg.jwt_secret, GET_PUBKEYS_PATH, None)?;
+    let response = client.get(&url).bearer_auth(&jwt).send().await?;
+    assert!(response.status() == StatusCode::TOO_MANY_REQUESTS);
+
+    // Wait until the cleanup task should have run properly, takes a while for the
+    // timing to work out
+    tokio::time::sleep(Duration::from_secs(
+        (start_config.jwt_auth_fail_timeout_seconds * 3) as u64,
+    ))
+    .await;
+
+    // Make sure the cleanup message was logged - it's all internal state so without
+    // refactoring or exposing it, this is the easiest way to check if it triggered
+    assert!(logs_contain("Cleaned up 1 old JWT auth failure entries"));
+
+    Ok(())
+}