diff --git a/src/_cffi_src/build_openssl.py b/src/_cffi_src/build_openssl.py
index 361473679ece..73bf02111090 100644
--- a/src/_cffi_src/build_openssl.py
+++ b/src/_cffi_src/build_openssl.py
@@ -26,6 +26,7 @@
         "asn1",
         "bignum",
         "bio",
+        "chacha",
         "cmac",
         "crypto",
         "dh",
diff --git a/src/_cffi_src/openssl/chacha.py b/src/_cffi_src/openssl/chacha.py
new file mode 100644
index 000000000000..7dff166fd08b
--- /dev/null
+++ b/src/_cffi_src/openssl/chacha.py
@@ -0,0 +1,42 @@
+# This file is dual licensed under the terms of the Apache License, Version
+# 2.0, and the BSD License. See the LICENSE file in the root of this repository
+# for complete details.
+
+from __future__ import annotations
+
+INCLUDES = """
+#if CRYPTOGRAPHY_IS_LIBRESSL
+#include <openssl/chacha.h>
+#endif"""
+
+TYPES = """
+static const long Cryptography_HAS_CHACHA20_API;
+"""
+
+FUNCTIONS = """
+/* Signature is different between LibreSSL and BoringSSL, so expose via
+   different symbol name */
+void Cryptography_CRYPTO_chacha_20(uint8_t *, const uint8_t *, size_t,
+                                   const uint8_t[32], const uint8_t[8],
+                                   uint64_t);
+"""
+
+CUSTOMIZATIONS = """
+#if CRYPTOGRAPHY_IS_LIBRESSL
+static const long Cryptography_HAS_CHACHA20_API = 1;
+#else
+static const long Cryptography_HAS_CHACHA20_API = 0;
+#endif
+
+#if CRYPTOGRAPHY_IS_LIBRESSL
+void Cryptography_CRYPTO_chacha_20(uint8_t *out, const uint8_t *in,
+                                   size_t in_len, const uint8_t key[32],
+                                   const uint8_t nonce[8], uint64_t counter) {
+    CRYPTO_chacha_20(out, in, in_len, key, nonce, counter);
+}
+#else
+void (*Cryptography_CRYPTO_chacha_20)(uint8_t *, const uint8_t *, size_t,
+                                      const uint8_t[32], const uint8_t[8],
+                                      uint64_t) = NULL;
+#endif
+"""
diff --git a/src/cryptography/hazmat/backends/openssl/backend.py b/src/cryptography/hazmat/backends/openssl/backend.py
index 3797d1df83e3..cbe68570ba58 100644
--- a/src/cryptography/hazmat/backends/openssl/backend.py
+++ b/src/cryptography/hazmat/backends/openssl/backend.py
@@ -12,7 +12,10 @@
 from cryptography import utils, x509
 from cryptography.exceptions import UnsupportedAlgorithm, _Reasons
 from cryptography.hazmat.backends.openssl import aead
-from cryptography.hazmat.backends.openssl.ciphers import _CipherContext
+from cryptography.hazmat.backends.openssl.ciphers import (
+    _CipherContext,
+    create_cipher_context,
+)
 from cryptography.hazmat.backends.openssl.cmac import _CMACContext
 from cryptography.hazmat.bindings._rust import openssl as rust_openssl
 from cryptography.hazmat.bindings.openssl import binding
@@ -221,6 +224,10 @@ def hmac_supported(self, algorithm: hashes.HashAlgorithm) -> bool:
         return self.hash_supported(algorithm)
 
     def cipher_supported(self, cipher: CipherAlgorithm, mode: Mode) -> bool:
+        # ChaCha20 is supported in LibreSSL by a different API than OpenSSL,
+        # so checking for the corresponding EVP_CIPHER is not useful
+        if self._lib.CRYPTOGRAPHY_IS_LIBRESSL and isinstance(cipher, ChaCha20):
+            return True
         if self._fips_enabled:
             # FIPS mode requires AES. TripleDES is disallowed/deprecated in
             # FIPS 140-3.
@@ -312,12 +319,12 @@ def _register_default_ciphers(self) -> None:
     def create_symmetric_encryption_ctx(
         self, cipher: CipherAlgorithm, mode: Mode
     ) -> _CipherContext:
-        return _CipherContext(self, cipher, mode, _CipherContext._ENCRYPT)
+        return create_cipher_context(self, cipher, mode, encrypt=True)
 
     def create_symmetric_decryption_ctx(
         self, cipher: CipherAlgorithm, mode: Mode
     ) -> _CipherContext:
-        return _CipherContext(self, cipher, mode, _CipherContext._DECRYPT)
+        return create_cipher_context(self, cipher, mode, encrypt=False)
 
     def pbkdf2_hmac_supported(self, algorithm: hashes.HashAlgorithm) -> bool:
         return self.hmac_supported(algorithm)
diff --git a/src/cryptography/hazmat/backends/openssl/ciphers.py b/src/cryptography/hazmat/backends/openssl/ciphers.py
index a34dcbe6ce1a..e6568767b166 100644
--- a/src/cryptography/hazmat/backends/openssl/ciphers.py
+++ b/src/cryptography/hazmat/backends/openssl/ciphers.py
@@ -4,6 +4,7 @@
 
 from __future__ import annotations
 
+import abc
 import typing
 
 from cryptography.exceptions import InvalidTag, UnsupportedAlgorithm, _Reasons
@@ -14,7 +15,175 @@
     from cryptography.hazmat.backends.openssl.backend import Backend
 
 
-class _CipherContext:
+class _CipherContext(metaclass=abc.ABCMeta):
+    _mode: typing.Any
+    tag: typing.Any
+
+    @abc.abstractmethod
+    def update(self, data: bytes) -> bytes:
+        """
+        Processes the provided bytes through the cipher and returns the results
+        as bytes.
+        """
+
+    @abc.abstractmethod
+    def update_into(self, data: bytes, buf: bytes) -> int:
+        """
+        Processes the provided bytes and writes the resulting data into the
+        provided buffer. Returns the number of bytes written.
+        """
+
+    @abc.abstractmethod
+    def finalize(self) -> bytes:
+        """
+        Returns the results of processing the final block as bytes.
+        """
+
+    @abc.abstractmethod
+    def authenticate_additional_data(self, data: bytes) -> None:
+        ...
+
+    @abc.abstractmethod
+    def finalize_with_tag(self, tag: bytes) -> bytes:
+        ...
+
+
+def create_cipher_context(
+    backend: Backend, cipher, mode: modes.Mode, encrypt: bool
+) -> _CipherContext:
+    if (
+        isinstance(cipher, algorithms.ChaCha20)
+        and backend._lib.Cryptography_HAS_CHACHA20_API
+    ):
+        return _CipherContextChaCha(backend, cipher)
+    else:
+        operation = (
+            _CipherContextEVP._ENCRYPT
+            if encrypt
+            else _CipherContextEVP._DECRYPT
+        )
+        return _CipherContextEVP(backend, cipher, mode, operation)
+
+
+class _CipherContextChaCha(_CipherContext):
+    """
+    Cipher context specific to ChaCha20 under LibreSSL
+    """
+
+    _BLOCK_SIZE_BYTES = 64
+    _MAX_COUNTER_VALUE = 2**64 - 1
+
+    def __init__(self, backend: Backend, cipher) -> None:
+        assert isinstance(cipher, algorithms.ChaCha20)
+        assert backend._lib.Cryptography_HAS_CHACHA20_API
+        self._backend = backend
+        self._cipher = cipher
+
+        # The ChaCha20 stream cipher. The key length is 256 bits, the IV is
+        # 128 bits long. The first 64 bits consists of a counter in
+        # little-endian order followed by a 64 bit nonce.
+        self._counter = int.from_bytes(cipher.nonce[:8], byteorder="little")
+        self._iv_nonce = cipher.nonce[8:]
+
+        # We store the cleartext of the last partial block encrypted. For
+        # example, if `update()` is called with 96 bytes of data (1.5 blocks),
+        # it will return all 96 bytes of ciphertext, but the last 32 bytes
+        # (0.5 blocks) will also be stored in `_leftover_data`.
+        # See `update_into()` for more details.
+        self._leftover_data = bytearray()
+
+    def update(self, data: bytes) -> bytes:
+        buf = bytearray(len(data))
+        n = self.update_into(data, buf)
+        return bytes(buf[:n])
+
+    def update_into(self, data: bytes, buf: bytes) -> int:
+        data_len = len(data)
+        if len(buf) < data_len:
+            raise ValueError(
+                f"buffer must be at least {data_len} bytes for this payload"
+            )
+
+        previous_leftover_len = len(self._leftover_data)
+        if previous_leftover_len > 0:
+            # We prepend the last partial block from previous `update_into()`
+            # calls so that the resulting ciphertext is the same as if the
+            # data had been passed as a full block.
+            # This is needed because LibreSSL and BoringSSL's ChaCha20 API is
+            # stateless, as opposed to OpenSSL's.
+            data_with_leftover = b"".join((self._leftover_data, data))
+            buffer_with_leftover: bytes | bytearray = bytearray(
+                len(data_with_leftover)
+            )
+        else:
+            data_with_leftover = data
+            buffer_with_leftover = buf
+
+        baseoutbuf = self._backend._ffi.from_buffer(
+            buffer_with_leftover, require_writable=True
+        )
+        baseinbuf = self._backend._ffi.from_buffer(data_with_leftover)
+
+        self._backend._lib.Cryptography_CRYPTO_chacha_20(
+            baseoutbuf,
+            baseinbuf,
+            len(data_with_leftover),
+            self._backend._ffi.from_buffer(self._cipher.key),
+            self._backend._ffi.from_buffer(self._iv_nonce),
+            self._counter,
+        )
+
+        if previous_leftover_len > 0:
+            # Since we had to use a new buffer different that `buf` to fit
+            # the ciphertext, now we need to copy the ciphertext to `buf`.
+            # We copy the ciphertext but skipping the bytes corresponding
+            # to `_leftover_buf`, since those have already been returned by a
+            # previous call.
+            self._backend._ffi.memmove(
+                buf,
+                buffer_with_leftover[previous_leftover_len:],
+                data_len,
+            )
+
+        complete_blocks_written, leftover_len = divmod(
+            len(data_with_leftover), self._BLOCK_SIZE_BYTES
+        )
+        if leftover_len > 0:
+            # Store the last partial block of data to use in the next call
+            self._leftover_data = bytearray(
+                data_with_leftover[
+                    complete_blocks_written * self._BLOCK_SIZE_BYTES :
+                ]
+            )
+            assert len(self._leftover_data) < 64
+        else:
+            self._leftover_data = bytearray()
+
+        # Our implementation of ChaCha20 uses a 64-bit counter which wraps
+        # around on overflow
+        self._counter += complete_blocks_written
+        if self._counter > self._MAX_COUNTER_VALUE:
+            self._counter -= self._MAX_COUNTER_VALUE + 1
+
+        return data_len
+
+    def finalize(self) -> bytes:
+        self._counter = 0
+        self._leftover_data = bytearray()
+        return b""
+
+    def authenticate_additional_data(self, data: bytes) -> None:
+        raise NotImplementedError(
+            "ChaCha20 context cannot be used as AEAD context"
+        )
+
+    def finalize_with_tag(self, tag: bytes) -> bytes:
+        raise NotImplementedError(
+            "ChaCha20 context cannot be used as AEAD context"
+        )
+
+
+class _CipherContextEVP(_CipherContext):
     _ENCRYPT = 1
     _DECRYPT = 0
     _MAX_CHUNK_SIZE = 2**30 - 1
diff --git a/tests/hazmat/backends/test_openssl.py b/tests/hazmat/backends/test_openssl.py
index 68f3d1a5fb24..8b2b9d0b0975 100644
--- a/tests/hazmat/backends/test_openssl.py
+++ b/tests/hazmat/backends/test_openssl.py
@@ -14,7 +14,7 @@
 from cryptography.hazmat.primitives import hashes, serialization
 from cryptography.hazmat.primitives.asymmetric import padding
 from cryptography.hazmat.primitives.ciphers import Cipher
-from cryptography.hazmat.primitives.ciphers.algorithms import AES
+from cryptography.hazmat.primitives.ciphers.algorithms import AES, ChaCha20
 from cryptography.hazmat.primitives.ciphers.modes import CBC
 
 from ...doubles import (
@@ -406,3 +406,25 @@ def test_public_load_dhx_unsupported(self, key_path, loader_func, backend):
         )
         with pytest.raises(ValueError):
             loader_func(key_bytes, backend)
+
+
+@pytest.mark.supported(
+    only_if=lambda backend: backend.cipher_supported(
+        ChaCha20(b"\x00" * 32, b"\x00" * 16), None
+    )
+    and backend._lib.CRYPTOGRAPHY_IS_LIBRESSL,
+    skip_message="Does not support non-EVP ChaCha20 cipher",
+)
+class TestChaCha20CipherContext:
+    def test_unsupported_api(self):
+        from cryptography.hazmat.backends.openssl.ciphers import (
+            _CipherContextChaCha,
+        )
+
+        ctx = _CipherContextChaCha(
+            backend, ChaCha20(b"\x00" * 32, b"\x00" * 16)
+        )
+        with pytest.raises(NotImplementedError):
+            ctx.authenticate_additional_data(b"data")
+        with pytest.raises(NotImplementedError):
+            ctx.finalize_with_tag(b"tag")
diff --git a/tests/hazmat/primitives/test_chacha20.py b/tests/hazmat/primitives/test_chacha20.py
index 314b0aa60666..7c52ad598d3c 100644
--- a/tests/hazmat/primitives/test_chacha20.py
+++ b/tests/hazmat/primitives/test_chacha20.py
@@ -69,3 +69,24 @@ def test_invalid_nonce(self):
     def test_invalid_key_type(self):
         with pytest.raises(TypeError, match="key must be bytes"):
             algorithms.ChaCha20("0" * 32, b"0" * 16)  # type:ignore[arg-type]
+
+    def test_partial_blocks(self, backend):
+        # Test that partial blocks and counter increments are handled
+        # correctly. Successive calls to update should return the same
+        # as if the entire input was passed in a single call:
+        # update(pt[0:n]) + update(pt[n:m]) + update(pt[m:]) == update(pt)
+        key = bytearray(os.urandom(32))
+        nonce = bytearray(os.urandom(16))
+        cipher = Cipher(algorithms.ChaCha20(key, nonce), None, backend)
+        pt = bytearray(os.urandom(96 * 3))
+
+        enc_full = cipher.encryptor()
+        ct_full = enc_full.update(pt)
+
+        enc_partial = cipher.encryptor()
+        len_partial = len(pt) // 3
+        ct_partial_1 = enc_partial.update(pt[:len_partial])
+        ct_partial_2 = enc_partial.update(pt[len_partial : len_partial * 2])
+        ct_partial_3 = enc_partial.update(pt[len_partial * 2 :])
+
+        assert ct_full == ct_partial_1 + ct_partial_2 + ct_partial_3
diff --git a/tests/hazmat/primitives/test_ciphers.py b/tests/hazmat/primitives/test_ciphers.py
index bf3b047dec25..9310550f5c45 100644
--- a/tests/hazmat/primitives/test_ciphers.py
+++ b/tests/hazmat/primitives/test_ciphers.py
@@ -15,6 +15,7 @@
     AES,
     ARC4,
     Camellia,
+    ChaCha20,
     TripleDES,
     _BlowfishInternal,
     _CAST5Internal,
@@ -340,6 +341,22 @@ def test_update_into_buffer_too_small_gcm(self, backend):
         with pytest.raises(ValueError):
             encryptor.update_into(b"testing", buf)
 
+    @pytest.mark.supported(
+        only_if=lambda backend: backend.cipher_supported(
+            ChaCha20(b"\x00" * 32, b"\x00" * 16), None
+        )
+        and backend._lib.CRYPTOGRAPHY_IS_LIBRESSL,
+        skip_message="Does not support non-EVP ChaCha20 cipher",
+    )
+    def test_update_into_buffer_too_small_chacha20(self, backend):
+        key = b"\x00" * 32
+        nonce = b"\x00" * 16
+        c = ciphers.Cipher(ChaCha20(key, nonce), None)
+        encryptor = c.encryptor()
+        buf = bytearray(5)
+        with pytest.raises(ValueError):
+            encryptor.update_into(b"testing", buf)
+
     def test_update_into_auto_chunking(self, backend, monkeypatch):
         key = b"\x00" * 16
         c = ciphers.Cipher(AES(key), modes.ECB(), backend)