diff --git a/backend/Cargo.lock b/backend/Cargo.lock
index d77be5e976..941c3c29ee 100644
--- a/backend/Cargo.lock
+++ b/backend/Cargo.lock
@@ -15618,6 +15618,7 @@ dependencies = [
  "serde_yml",
  "sha2 0.10.9",
  "size",
+ "spki",
  "sqlx",
  "strum",
  "strum_macros",
diff --git a/backend/Cargo.toml b/backend/Cargo.toml
index 25f2165bd2..e58cb3f5d0 100644
--- a/backend/Cargo.toml
+++ b/backend/Cargo.toml
@@ -600,6 +600,7 @@ const_format = { version = "0.2.35", features = ["rust_1_64", "rust_1_51"] }
 const-str = "0.5"
 constant_time_eq = "0.3.1"
 rsa = "^0"
+spki = { version = "0.7", features = ["pem"] }
 aes-gcm = "0.10.3"
 async_zip = { version = "0.0.17", features = ["tokio", "tokio-fs", "deflate", "chrono"] }
 once_cell = "1.17.1"
diff --git a/backend/windmill-common/Cargo.toml b/backend/windmill-common/Cargo.toml
index e2c3233183..76b7b8cbf3 100644
--- a/backend/windmill-common/Cargo.toml
+++ b/backend/windmill-common/Cargo.toml
@@ -109,6 +109,7 @@ pep440_rs.workspace = true
 systemstat.workspace = true
 size.workspace = true
 rsa = { workspace = true, optional = true }
+spki = { workspace = true }
 aes-gcm = { workspace = true, optional = true }
 
 semver.workspace = true
diff --git a/backend/windmill-common/src/guest_jwt.rs b/backend/windmill-common/src/guest_jwt.rs
index c82f5ac06e..d496cc6a01 100644
--- a/backend/windmill-common/src/guest_jwt.rs
+++ b/backend/windmill-common/src/guest_jwt.rs
@@ -80,15 +80,20 @@ pub async fn key_source(db: &DB, w_id: &str) -> Result<Option<GuestJwtKeySource>
 /// EC keys the ES family. Anything symmetric has no PEM form, so HS* is unreachable
 /// from here by construction; the JWKS path refuses it explicitly.
 pub fn decoding_key_from_pem(pem: &str) -> Result<(DecodingKey, &'static [Algorithm])> {
+    use spki::der::{Decode, Document};
     let pem = pem.trim();
-    // A verification key must be public. jsonwebtoken 8.3's `from_rsa_pem` also accepts private
-    // encodings (PKCS#1, PKCS#8), so a pasted private key would be stored and then served back
-    // through the settings response. Refuse any private PEM before it is parsed or persisted.
-    if pem.contains("PRIVATE KEY") {
-        return Err(Error::BadRequest(
-            "expected a PEM public key (-----BEGIN PUBLIC KEY-----), not a private key".to_string(),
-        ));
-    }
+    // A verification key must be public. jsonwebtoken 8.3 keys the public/private distinction
+    // off the PEM label alone and never inspects the DER, so private material relabelled
+    // `PUBLIC KEY` would be stored and then served back through the settings response. Require
+    // the key to parse as a SubjectPublicKeyInfo, which private-key DER cannot satisfy.
+    let (_, doc) = Document::from_pem(pem)
+        .map_err(|e| Error::BadRequest(format!("not a valid PEM key: {e}")))?;
+    spki::SubjectPublicKeyInfoRef::from_der(doc.as_bytes()).map_err(|_| {
+        Error::BadRequest(
+            "expected an RSA or EC public key in SPKI form (-----BEGIN PUBLIC KEY-----)"
+                .to_string(),
+        )
+    })?;
     if let Ok(key) = DecodingKey::from_rsa_pem(pem.as_bytes()) {
         return Ok((key, &RSA_ALGORITHMS));
     }
@@ -533,16 +538,61 @@ mod tests {
         .is_err());
     }
 
+    // A real RSA public key (SPKI). Its private counterpart is RSA_PKCS1_PRIVATE below.
+    const RSA_PUBLIC: &str = "-----BEGIN PUBLIC KEY-----\n\
+MIIBIjANBgkqhkiG9w0BAQEFAAOCAQ8AMIIBCgKCAQEAx3J0fQcHp2ZlMI4rCVsY\n\
+tirATZPWyPD7exoYWPInhV5xjbY2Fe8IVFaZszQcQbCXZjBtFp2fj0tBTow8BeOy\n\
+X9LJPyKeho/j68FycuDVg7JCzG0TWtsnh/V23WkrlKIfmMqS3+YUyFavROTcAN1T\n\
+5BcFHLAi/4Q2qy0JjXBdZ8avelzZrQ/T67/Kcsoct/pvnEDT2YRsSbA7VMWaxWh8\n\
+MYJ7GNV/10YT2c5CBJGSLbyRSVWk2IwfnM9Cl9n/5NE6TkSetYQ2xlqKTONp5W43\n\
+UzW1NAeqKCxPQfN/ADjwW18nk2o7xj1kMF4rBlhsTm9ClE71nwi5NxsvMOdVxytZ\n\
+ZQIDAQAB\n\
+-----END PUBLIC KEY-----\n";
+
+    // A complete, valid PKCS#1 RSA *private* key (the counterpart of RSA_PUBLIC) with its
+    // armor relabelled `RSA PUBLIC KEY`. jsonwebtoken's from_rsa_pem accepts it under that
+    // label; the SPKI parse is what refuses it. Complete on purpose: malformed DER would fail
+    // for the wrong reason and let a real bypass through unnoticed.
+    const RSA_PKCS1_PRIVATE_AS_PUBLIC: &str = "-----BEGIN RSA PUBLIC KEY-----\n\
+MIIEogIBAAKCAQEAx3J0fQcHp2ZlMI4rCVsYtirATZPWyPD7exoYWPInhV5xjbY2\n\
+Fe8IVFaZszQcQbCXZjBtFp2fj0tBTow8BeOyX9LJPyKeho/j68FycuDVg7JCzG0T\n\
+Wtsnh/V23WkrlKIfmMqS3+YUyFavROTcAN1T5BcFHLAi/4Q2qy0JjXBdZ8avelzZ\n\
+rQ/T67/Kcsoct/pvnEDT2YRsSbA7VMWaxWh8MYJ7GNV/10YT2c5CBJGSLbyRSVWk\n\
+2IwfnM9Cl9n/5NE6TkSetYQ2xlqKTONp5W43UzW1NAeqKCxPQfN/ADjwW18nk2o7\n\
+xj1kMF4rBlhsTm9ClE71nwi5NxsvMOdVxytZZQIDAQABAoIBAD+IbaQQM7d3Dj/X\n\
+4cyyqJ4K40QzFmXfIfTWXLAkv0MkUR7XzsXQ5YHcLkzgCipAwxGp1m4wWs4OJmkL\n\
+kek8XatZnYLPl9j8iBmm/zqp9Unk5JNzIYm9KwwLvMgOAvRvaopE6WGKTM9+kYls\n\
+L8rUti7/yECZuSRU7Qc9KwBTrWVrXK+RBtBqZYQXb92BFxq0N3Qp+utLNdFcO5sW\n\
+7d8gKp3ipQt5z9ZAB2pYMw7ZTzonF4C7HdyrbYXztvYrxuw1imMkQ9iFFhdn3/76\n\
+qFR7XwaFrld8DECGaH/652kV6zaSQijbBTeXF4zsgwXY4BHMVmZKaXH5unw8Gbmo\n\
+WCoLbLcCgYEA4vTo5kCiKXnlBp3W1Zpg4cml6Wzo0UDldF4kkuXQxhdQA38c0ise\n\
+Cocf6qyAqz1L2TxQ/9WCL2oIP1AY9XqnQ0cJtYIosGWORz4tPe67M8inB/GBotFI\n\
+pmQNVSIjqbgKVi0x+UzmFjitINFPf461lDdJTwhsv9TQRbHrXErvON8CgYEA4PhV\n\
+GYMJu46tqFVtD/koWAQRLmeaZXhxP5lMSmQjdYCa3ys5lccvTlzoF9K8immMQkIx\n\
+gyOazmEtFnK4IXmEY1wg2NIHuJM7/maoM2rozbjXBxsYM7Xw2QX7BHXqG6Ia/Bij\n\
+ZaRJdumCVRJv7OshQTGuqDIzd3l5WEqg11XYgjsCgYAP3v6Wc3ijm+GXN9x5LYWO\n\
+5JIUo8gYMgiZvaejGi0iXSj8RZxXWiqMo+xodc29q9itBVnIuj6TYD/ZZZmJOR2P\n\
+R9128vYzd7aeZsu1JAe1VFfR52KgZzBEaoTAKlYCHVujsR9ohqckcKwyulBr5Cfw\n\
+iHk47KbmN1SlOw7xclAOUwKBgAuxHEsdIk5bFe9fsTFZU51vaK0uuTl4zvntL6fW\n\
+GHms21+p0W5VUcIS1gUW8LGI1r9CzWvxV8RODJfUEnm65QR870AVek0/aajJEQjL\n\
+D5pRdutpnxJg7El7JBaRQj95Z0mexi8sIJ1LeXiOYr6/YZUPzfHz2fTlnUbXahCG\n\
+55+tAoGAI811NTb7kuuIPYuj4raDW88QVNX2xB3+p9lXGolB4jPgsUEjgSvLgH9S\n\
+Q/LwEBiCYVyii8MvWsIZpHvSGyOoty2p19/CAvrAOfpEVlnXQeiX+mh09p1mQbfM\n\
+y9rTR828ADcaZ63Ej1oL4GcqmGhODxCLy1YKKcy0FHzChqPMV6g=\n\
+-----END RSA PUBLIC KEY-----\n";
+
     #[test]
     fn a_private_pem_is_refused() {
-        // A verification key must be public; a private key must never be stored, as it is
-        // served back through the settings response. PRIV1 is a real EC private key the PEM
-        // parser would otherwise accept; the RSA label covers jsonwebtoken's PKCS#1/#8 case.
+        // A verification key must be public and must never be stored otherwise: it is served
+        // back through the settings response. jsonwebtoken keys the public/private split off
+        // the PEM label, so private DER relabelled with a public armor slips a label check;
+        // only parsing the DER as a SubjectPublicKeyInfo refuses it. A real public key still
+        // parses, so the guard is not vacuous.
+        assert!(decoding_key_from_pem(RSA_PUBLIC).is_ok());
         assert!(decoding_key_from_pem(PRIV1).is_err());
-        assert!(decoding_key_from_pem(
-            "-----BEGIN RSA PRIVATE KEY-----\nMIIBOgIBAAJBAKj\n-----END RSA PRIVATE KEY-----\n"
-        )
-        .is_err());
+        // The same PKCS#8 EC private key, relabelled `PUBLIC KEY`.
+        assert!(decoding_key_from_pem(&PRIV1.replace("PRIVATE KEY", "PUBLIC KEY")).is_err());
+        assert!(decoding_key_from_pem(RSA_PKCS1_PRIVATE_AS_PUBLIC).is_err());
     }
 
     #[tokio::test]