diff --git a/src/crypto/crypto_sig.cc b/src/crypto/crypto_sig.cc
index 64e788dcecaca1..a0ed640acaaa89 100644
--- a/src/crypto/crypto_sig.cc
+++ b/src/crypto/crypto_sig.cc
@@ -420,6 +420,11 @@ void Sign::SignFinal(const FunctionCallbackInfo<Value>& args) {
   if (!key)
     return;
 
+  if (IsOneShot(key)) {
+    THROW_ERR_CRYPTO_UNSUPPORTED_OPERATION(env);
+    return;
+  }
+
   int padding = GetDefaultSignPadding(key);
   if (!args[offset]->IsUndefined()) {
     CHECK(args[offset]->IsInt32());
@@ -547,6 +552,11 @@ void Verify::VerifyFinal(const FunctionCallbackInfo<Value>& args) {
   if (!pkey)
     return;
 
+  if (IsOneShot(pkey)) {
+    THROW_ERR_CRYPTO_UNSUPPORTED_OPERATION(env);
+    return;
+  }
+
   ArrayBufferOrViewContents<char> hbuf(args[offset]);
   if (UNLIKELY(!hbuf.CheckSizeInt32()))
     return THROW_ERR_OUT_OF_RANGE(env, "buffer is too big");
diff --git a/test/parallel/test-crypto-sign-verify.js b/test/parallel/test-crypto-sign-verify.js
index 74c0ff53eb18b7..81adde1ba771c8 100644
--- a/test/parallel/test-crypto-sign-verify.js
+++ b/test/parallel/test-crypto-sign-verify.js
@@ -774,3 +774,23 @@ assert.throws(
     }, { code: 'ERR_INVALID_ARG_TYPE', message: /The "key\.key" property must be of type object/ });
   }
 }
+
+{
+  // Ed25519 and Ed448 must use the one-shot methods
+  const keys = [{ privateKey: fixtures.readKey('ed25519_private.pem', 'ascii'),
+                  publicKey: fixtures.readKey('ed25519_public.pem', 'ascii') },
+                { privateKey: fixtures.readKey('ed448_private.pem', 'ascii'),
+                  publicKey: fixtures.readKey('ed448_public.pem', 'ascii') }];
+
+  for (const { publicKey, privateKey } of keys) {
+    assert.throws(() => {
+      crypto.createSign('SHA256').update('Test123').sign(privateKey);
+    }, { code: 'ERR_CRYPTO_UNSUPPORTED_OPERATION', message: 'Unsupported crypto operation' });
+    assert.throws(() => {
+      crypto.createVerify('SHA256').update('Test123').verify(privateKey, 'sig');
+    }, { code: 'ERR_CRYPTO_UNSUPPORTED_OPERATION', message: 'Unsupported crypto operation' });
+    assert.throws(() => {
+      crypto.createVerify('SHA256').update('Test123').verify(publicKey, 'sig');
+    }, { code: 'ERR_CRYPTO_UNSUPPORTED_OPERATION', message: 'Unsupported crypto operation' });
+  }
+}