diff --git a/ext/openssl/ossl_cipher.c b/ext/openssl/ossl_cipher.c
index db08b9374d9..ba58594b7be 100644
--- a/ext/openssl/ossl_cipher.c
+++ b/ext/openssl/ossl_cipher.c
@@ -325,6 +325,9 @@ ossl_cipher_update_long(EVP_CIPHER_CTX *ctx, unsigned char *out,
     int limit = INT_MAX / 2 + 1;
     rb_len_t out_len = 0;
 
+    if (out == in && in_len > limit)
+        ossl_raise(eCipherError, "input too large for in-place update");
+
     do {
         int in_part_len = in_len > limit ? limit : (int)in_len;
 
@@ -361,19 +364,19 @@ static VALUE
 ossl_cipher_update(int argc, VALUE *argv, VALUE self)
 {
     EVP_CIPHER_CTX *ctx;
-    unsigned char *in;
     rb_len_t in_len, out_len;
     VALUE data, str;
 
     rb_scan_args(argc, argv, "11", &data, &str);
+    GetCipher(self, ctx);
 
     if (!RTEST(rb_attr_get(self, id_key_set)))
         ossl_raise(eCipherError, "key not set");
 
     StringValue(data);
-    in = (unsigned char *)RSTRING_PTR(data);
+    if (!NIL_P(str))
+        StringValue(str);
     in_len = RSTRING_LEN(data);
-    GetCipher(self, ctx);
 
     /*
      * As of OpenSSL 3.2, there is no reliable way to determine the required
@@ -396,15 +399,15 @@ ossl_cipher_update(int argc, VALUE *argv, VALUE self)
     if (NIL_P(str))
         str = rb_str_buf_new(out_len);
     else {
-        StringValue(str);
         if ((rb_len_t)rb_str_capacity(str) >= out_len)
             rb_str_modify(str);
         else
             rb_str_modify_expand(str, out_len - RSTRING_LEN(str));
     }
 
-    if (!ossl_cipher_update_long(ctx, (unsigned char *)RSTRING_PTR(str),
-                                 &out_len, in, in_len))
+    if (!ossl_cipher_update_long(ctx,
+                                 (unsigned char *)RSTRING_PTR(str), &out_len,
+                                 (unsigned char *)RSTRING_PTR(data), in_len))
         ossl_raise(eCipherError, "EVP_CipherUpdate");
     rb_str_set_len(str, out_len);
 
diff --git a/test/openssl/test_cipher.rb b/test/openssl/test_cipher.rb
index b7926780c5b..890dc760d58 100644
--- a/test/openssl/test_cipher.rb
+++ b/test/openssl/test_cipher.rb
@@ -117,7 +117,7 @@ class OpenSSL::TestCipher < OpenSSL::TestCase
     }
   end
 
-  def test_ctr_if_exists
+  def test_aes_ctr
     # NIST SP 800-38A F.5.1
     key = ["2b7e151628aed2a6abf7158809cf4f3c"].pack("H*")
     iv =  ["f0f1f2f3f4f5f6f7f8f9fafbfcfdfeff"].pack("H*")
@@ -125,10 +125,16 @@ class OpenSSL::TestCipher < OpenSSL::TestCase
            "ae2d8a571e03ac9c9eb76fac45af8e51"].pack("H*")
     ct =  ["874d6191b620e3261bef6864990db6ce" \
            "9806f66b7970fdff8617187bb9fffdff"].pack("H*")
-    cipher = new_encryptor("aes-128-ctr", key: key, iv: iv, padding: 0)
+    cipher = new_encryptor("aes-128-ctr", key: key, iv: iv)
     assert_equal ct, cipher.update(pt) << cipher.final
-    cipher = new_decryptor("aes-128-ctr", key: key, iv: iv, padding: 0)
+    cipher = new_decryptor("aes-128-ctr", key: key, iv: iv)
     assert_equal pt, cipher.update(ct) << cipher.final
+
+    # in-place update
+    cipher = new_encryptor("aes-128-ctr", key: key, iv: iv)
+    buf = Marshal.load(Marshal.dump(pt))
+    assert_equal(ct, cipher.update(buf, buf))
+    assert_equal(ct, buf)
   end
 
   def test_update_with_buffer