diff --git a/Cargo.lock b/Cargo.lock
index c7ffffd97ba..b45ed61909d 100644
--- a/Cargo.lock
+++ b/Cargo.lock
@@ -6072,6 +6072,7 @@ version = "1.0.0-beta.40"
 dependencies = [
  "base64 0.22.1",
  "chrono",
+ "color-eyre",
  "futures",
  "hex",
  "indexmap 2.5.0",
diff --git a/zebra-rpc/Cargo.toml b/zebra-rpc/Cargo.toml
index 37349b34d8c..d3976e15e1e 100644
--- a/zebra-rpc/Cargo.toml
+++ b/zebra-rpc/Cargo.toml
@@ -71,6 +71,9 @@ indexmap = { version = "2.5.0", features = ["serde"] }
 base64 = "0.22.1"
 rand = "0.8.5"
 
+# Error handling
+color-eyre = "0.6.3"
+
 tokio = { version = "1.40.0", features = [
     "time",
     "rt-multi-thread",
diff --git a/zebra-rpc/src/server.rs b/zebra-rpc/src/server.rs
index a9b6dcfc6ac..9b12dad730d 100644
--- a/zebra-rpc/src/server.rs
+++ b/zebra-rpc/src/server.rs
@@ -194,8 +194,10 @@ impl RpcServer {
                 parallel_cpu_threads = available_parallelism().map(usize::from).unwrap_or(1);
             }
 
-            // generate a cookie
-            cookie::generate(config.cookie_dir.clone());
+            // Generate a RPC authentication cookie
+            if config.enable_cookie_auth {
+                let _ = cookie::generate(config.cookie_dir.clone());
+            }
 
             // The server is a blocking task, which blocks on executor shutdown.
             // So we need to start it in a std::thread.
@@ -303,7 +305,7 @@ impl RpcServer {
             span.in_scope(|| {
                 info!("Stopping RPC server");
                 close_handle.clone().close();
-                cookie::delete(); // delete the auth cookie
+                let _ = cookie::delete(); // delete the auth cookie if exists
                 debug!("Stopped RPC server");
             })
         };
diff --git a/zebra-rpc/src/server/cookie.rs b/zebra-rpc/src/server/cookie.rs
index cbcf7bd9f4e..213165a5cec 100644
--- a/zebra-rpc/src/server/cookie.rs
+++ b/zebra-rpc/src/server/cookie.rs
@@ -1,6 +1,7 @@
 //! Cookie-based authentication for the RPC server.
 
 use base64::{engine::general_purpose::URL_SAFE, Engine as _};
+use color_eyre::Result;
 use rand::RngCore;
 
 use std::{
@@ -14,34 +15,34 @@ pub const COOKIEAUTH_USER: &str = "__cookie__";
 /// Default name for auth cookie file */
 pub const COOKIEAUTH_FILE: &str = ".cookie";
 
-/// Generate a new auth cookie and return the encoded password.
-pub fn generate(cookie_dir: PathBuf) -> Option<()> {
+/// Generate a new auth cookie and store it in the given `cookie_dir`.
+pub fn generate(cookie_dir: PathBuf) -> Result<()> {
     let mut data = [0u8; 32];
     rand::thread_rng().fill_bytes(&mut data);
     let encoded_password = URL_SAFE.encode(data);
     let cookie_content = format!("{}:{}", COOKIEAUTH_USER, encoded_password);
 
-    let mut file = File::create(cookie_dir.join(COOKIEAUTH_FILE)).ok()?;
-    file.write_all(cookie_content.as_bytes()).ok()?;
+    let mut file = File::create(cookie_dir.join(COOKIEAUTH_FILE))?;
+    file.write_all(cookie_content.as_bytes())?;
 
     tracing::info!("RPC auth cookie generated successfully");
 
-    Some(())
+    Ok(())
 }
 
 /// Get the encoded password from the auth cookie.
-pub fn get(cookie_dir: PathBuf) -> Option<String> {
-    let mut file = File::open(cookie_dir.join(COOKIEAUTH_FILE)).ok()?;
+pub fn get(cookie_dir: PathBuf) -> Result<String> {
+    let mut file = File::open(cookie_dir.join(COOKIEAUTH_FILE))?;
     let mut contents = String::new();
-    file.read_to_string(&mut contents).ok()?;
+    file.read_to_string(&mut contents)?;
 
     let parts: Vec<&str> = contents.split(":").collect();
-    Some(parts[1].to_string())
+    Ok(parts[1].to_string())
 }
 
 /// Delete the auth cookie.
-pub fn delete() -> Option<()> {
-    remove_file(COOKIEAUTH_FILE).ok()?;
+pub fn delete() -> Result<()> {
+    remove_file(COOKIEAUTH_FILE)?;
     tracing::info!("RPC auth cookie deleted successfully");
-    Some(())
+    Ok(())
 }
diff --git a/zebra-rpc/src/server/http_request_compatibility.rs b/zebra-rpc/src/server/http_request_compatibility.rs
index 653edc791d5..b07f04ef29d 100644
--- a/zebra-rpc/src/server/http_request_compatibility.rs
+++ b/zebra-rpc/src/server/http_request_compatibility.rs
@@ -180,7 +180,7 @@ impl FixHttpRequestMiddleware {
                     .map(|password| password.to_string())
             })
             .map_or(false, |password| {
-                if let Some(cookie_password) = cookie::get(self.0.cookie_dir.clone()) {
+                if let Ok(cookie_password) = cookie::get(self.0.cookie_dir.clone()) {
                     cookie_password == password
                 } else {
                     false