diff --git a/Cargo.lock b/Cargo.lock
index 5d0ba1748..242d039f2 100644
--- a/Cargo.lock
+++ b/Cargo.lock
@@ -3220,6 +3220,7 @@ dependencies = [
  "chrono",
  "figment",
  "governor",
+ "hex",
  "indoc",
  "ipnetwork",
  "lettre",
diff --git a/crates/cli/src/commands/config.rs b/crates/cli/src/commands/config.rs
index 8416e5592..00600026c 100644
--- a/crates/cli/src/commands/config.rs
+++ b/crates/cli/src/commands/config.rs
@@ -123,7 +123,7 @@ impl Options {
             SC::Sync { prune, dry_run } => {
                 let config = SyncConfig::extract(figment)?;
                 let clock = SystemClock::default();
-                let encrypter = config.secrets.encrypter();
+                let encrypter = config.secrets.encrypter().await?;
 
                 // Grab a connection to the database
                 let mut conn = database_connection_from_config(&config.database).await?;
diff --git a/crates/cli/src/commands/server.rs b/crates/cli/src/commands/server.rs
index 4f2fc6205..dcdbca0d3 100644
--- a/crates/cli/src/commands/server.rs
+++ b/crates/cli/src/commands/server.rs
@@ -94,7 +94,7 @@ impl Options {
                 .context("could not run database migrations")?;
         }
 
-        let encrypter = config.secrets.encrypter();
+        let encrypter = config.secrets.encrypter().await?;
 
         if self.no_sync {
             info!("Skipping configuration sync");
@@ -124,8 +124,10 @@ impl Options {
             .await
             .context("could not import keys from config")?;
 
-        let cookie_manager =
-            CookieManager::derive_from(config.http.public_base.clone(), &config.secrets.encryption);
+        let cookie_manager = CookieManager::derive_from(
+            config.http.public_base.clone(),
+            &config.secrets.encryption().await?,
+        );
 
         // Load and compile the WASM policies (and fallback to the default embedded one)
         info!("Loading and compiling the policy module");
diff --git a/crates/cli/src/commands/syn2mas.rs b/crates/cli/src/commands/syn2mas.rs
index ac009f5cf..22194953e 100644
--- a/crates/cli/src/commands/syn2mas.rs
+++ b/crates/cli/src/commands/syn2mas.rs
@@ -133,7 +133,7 @@ impl Options {
             // in the MAS database
             let config = SyncConfig::extract(figment)?;
             let clock = SystemClock::default();
-            let encrypter = config.secrets.encrypter();
+            let encrypter = config.secrets.encrypter().await?;
 
             crate::sync::config_sync(
                 config.upstream_oauth2,
diff --git a/crates/config/Cargo.toml b/crates/config/Cargo.toml
index 7566b59c0..b44e958aa 100644
--- a/crates/config/Cargo.toml
+++ b/crates/config/Cargo.toml
@@ -19,6 +19,7 @@ anyhow.workspace = true
 camino = { workspace = true, features = ["serde1"] }
 chrono.workspace = true
 figment.workspace = true
+hex.workspace = true
 ipnetwork = { version = "0.20.0", features = ["serde", "schemars"] }
 lettre.workspace = true
 schemars.workspace = true
diff --git a/crates/config/src/sections/secrets.rs b/crates/config/src/sections/secrets.rs
index 10df52e02..341ea7150 100644
--- a/crates/config/src/sections/secrets.rs
+++ b/crates/config/src/sections/secrets.rs
@@ -46,18 +46,70 @@ pub struct KeyConfig {
     key_file: Option<Utf8PathBuf>,
 }
 
-/// Application secrets
+/// Encryption config option.
+#[derive(Debug, Clone)]
+pub enum Encryption {
+    File(Utf8PathBuf),
+    Value([u8; 32]),
+}
+
+/// Encryption fields as serialized in JSON.
 #[serde_as]
-#[derive(Debug, Clone, Serialize, Deserialize, JsonSchema)]
-pub struct SecretsConfig {
-    /// Encryption key for secure cookies
+#[derive(JsonSchema, Serialize, Deserialize, Debug, Clone)]
+struct EncryptionRaw {
+    /// File containing the encryption key for secure cookies.
+    #[schemars(with = "Option<String>")]
+    #[serde(skip_serializing_if = "Option::is_none")]
+    encryption_file: Option<Utf8PathBuf>,
+
+    /// Encryption key for secure cookies.
     #[schemars(
-        with = "String",
+        with = "Option<String>",
         regex(pattern = r"[0-9a-fA-F]{64}"),
         example = "example_secret"
     )]
-    #[serde_as(as = "serde_with::hex::Hex")]
-    pub encryption: [u8; 32],
+    #[serde_as(as = "Option<serde_with::hex::Hex>")]
+    #[serde(skip_serializing_if = "Option::is_none")]
+    encryption: Option<[u8; 32]>,
+}
+
+impl TryFrom<EncryptionRaw> for Encryption {
+    type Error = anyhow::Error;
+
+    fn try_from(value: EncryptionRaw) -> Result<Encryption, Self::Error> {
+        match (value.encryption, value.encryption_file) {
+            (None, None) => bail!("Missing `encryption` or `encryption_file`"),
+            (None, Some(path)) => Ok(Encryption::File(path)),
+            (Some(encryption), None) => Ok(Encryption::Value(encryption)),
+            (Some(_), Some(_)) => bail!("Cannot specify both `encryption` and `encryption_file`"),
+        }
+    }
+}
+
+impl From<Encryption> for EncryptionRaw {
+    fn from(value: Encryption) -> Self {
+        match value {
+            Encryption::File(path) => EncryptionRaw {
+                encryption_file: Some(path),
+                encryption: None,
+            },
+            Encryption::Value(encryption) => EncryptionRaw {
+                encryption_file: None,
+                encryption: Some(encryption),
+            },
+        }
+    }
+}
+
+/// Application secrets
+#[serde_as]
+#[derive(Debug, Clone, Serialize, Deserialize, JsonSchema)]
+pub struct SecretsConfig {
+    /// Encryption key for secure cookies
+    #[schemars(with = "EncryptionRaw")]
+    #[serde_as(as = "serde_with::TryFromInto<EncryptionRaw>")]
+    #[serde(flatten)]
+    encryption: Encryption,
 
     /// List of private keys to use for signing and encrypting payloads
     #[serde(default)]
@@ -118,9 +170,33 @@ impl SecretsConfig {
     }
 
     /// Derive an [`Encrypter`] out of the config
-    #[must_use]
-    pub fn encrypter(&self) -> Encrypter {
-        Encrypter::new(&self.encryption)
+    ///
+    /// # Errors
+    ///
+    /// Returns an error when the Encryptor can not be created.
+    pub async fn encrypter(&self) -> anyhow::Result<Encrypter> {
+        Ok(Encrypter::new(&self.encryption().await?))
+    }
+
+    /// Returns the encryption secret.
+    ///
+    /// # Errors
+    ///
+    /// Returns an error when the encryption secret could not be read from file.
+    pub async fn encryption(&self) -> anyhow::Result<[u8; 32]> {
+        // Read the encryption secret either embedded in the config file or on disk
+        match self.encryption {
+            Encryption::Value(encryption) => Ok(encryption),
+            Encryption::File(ref path) => {
+                let mut bytes = [0; 32];
+                let content = tokio::fs::read(path).await?;
+                hex::decode_to_slice(content, &mut bytes).context(
+                    "Content of `encryption_file` must contain hex characters \
+                    encoding exactly 32 bytes",
+                )?;
+                Ok(bytes)
+            }
+        }
     }
 }
 
@@ -246,7 +322,7 @@ impl SecretsConfig {
         };
 
         Ok(Self {
-            encryption: Standard.sample(&mut rng),
+            encryption: Encryption::Value(Standard.sample(&mut rng)),
             keys: vec![rsa_key, ec_p256_key, ec_p384_key, ec_k256_key],
         })
     }
@@ -291,7 +367,7 @@ impl SecretsConfig {
         };
 
         Self {
-            encryption: [0xEA; 32],
+            encryption: Encryption::Value([0xEA; 32]),
             keys: vec![rsa_key, ecdsa_key],
         }
     }
diff --git a/docs/config.schema.json b/docs/config.schema.json
index 3bc0f407d..6867dd8d2 100644
--- a/docs/config.schema.json
+++ b/docs/config.schema.json
@@ -1515,18 +1515,7 @@
     "SecretsConfig": {
       "description": "Application secrets",
       "type": "object",
-      "required": [
-        "encryption"
-      ],
       "properties": {
-        "encryption": {
-          "description": "Encryption key for secure cookies",
-          "examples": [
-            "0000111122223333444455556666777788889999aaaabbbbccccddddeeeeffff"
-          ],
-          "type": "string",
-          "pattern": "[0-9a-fA-F]{64}"
-        },
         "keys": {
           "description": "List of private keys to use for signing and encrypting payloads",
           "default": [],
@@ -1534,6 +1523,18 @@
           "items": {
             "$ref": "#/definitions/KeyConfig"
           }
+        },
+        "encryption_file": {
+          "description": "File containing the encryption key for secure cookies.",
+          "type": "string"
+        },
+        "encryption": {
+          "description": "Encryption key for secure cookies.",
+          "examples": [
+            "0000111122223333444455556666777788889999aaaabbbbccccddddeeeeffff"
+          ],
+          "type": "string",
+          "pattern": "[0-9a-fA-F]{64}"
         }
       }
     },
diff --git a/docs/reference/configuration.md b/docs/reference/configuration.md
index 2303e889e..628ec6c52 100644
--- a/docs/reference/configuration.md
+++ b/docs/reference/configuration.md
@@ -232,6 +232,21 @@ secrets:
         -----END EC PRIVATE KEY-----
 ```
 
+### `secrets.encryption{_file}`
+
+The encryption secret used for encrypting cookies and database fields. It takes
+the form of a 32-bytes-long hex-encoded string. To provide the encryption secret
+via file, set `secrets.encryption_file` to the file path; alternatively use
+`secrets.encryption` for declaring the secret inline. The options
+`secrets.encryption_file` and `secrets.encryption` are mutually exclusive.
+
+If given via file, the encyption secret is only read at application startup.
+The secret is not updated when the content of the file changes.
+
+> ⚠️ **Warning** – Do not change the encryption secret after the initial start!
+> Changing the encryption secret afterwards will lead to a loss of all encrypted
+> information in the database.
+
 ### `secrets.keys`
 
 The service can use a number of key types for signing.