diff --git a/src/crawlee/http_clients/_httpx.py b/src/crawlee/http_clients/_httpx.py
index ec3705a016..ae8d6304bb 100644
--- a/src/crawlee/http_clients/_httpx.py
+++ b/src/crawlee/http_clients/_httpx.py
@@ -284,6 +284,7 @@ def _build_request(
             method=method,
             headers=dict(headers) if headers else None,
             content=payload,
+            cookies=session.cookies.jar if session else None,
             extensions={'crawlee_session': session if self._persist_cookies_per_session else None},
             timeout=timeout or httpx.USE_CLIENT_DEFAULT,
         )
@@ -333,15 +334,19 @@ def _get_client(self, proxy_url: str | None) -> httpx.AsyncClient:
     def _combine_headers(self, explicit_headers: HttpHeaders | None) -> HttpHeaders | None:
         """Merge default headers with explicit headers for an HTTP request.
 
-        Generate a final set of request headers by combining default headers, a random User-Agent header,
-        and any explicitly provided headers.
+        Generate a final set of request headers by combining default headers from a single fingerprint
+        (Accept, Accept-Language, User-Agent) and any explicitly provided headers. Using one fingerprint
+        avoids mixing Accept headers from one browser profile with a User-Agent from another.
         """
-        common_headers = self._header_generator.get_common_headers() if self._header_generator else HttpHeaders()
-        user_agent_header = (
-            self._header_generator.get_random_user_agent_header() if self._header_generator else HttpHeaders()
-        )
+        if self._header_generator:
+            generated_headers = self._header_generator.get_specific_headers(
+                header_names={'Accept', 'Accept-Language', 'User-Agent'},
+            )
+        else:
+            generated_headers = HttpHeaders()
+
         explicit_headers = explicit_headers or HttpHeaders()
-        headers = common_headers | user_agent_header | explicit_headers
+        headers = generated_headers | explicit_headers
         return headers or None
 
     @staticmethod
diff --git a/src/crawlee/http_clients/_impit.py b/src/crawlee/http_clients/_impit.py
index 11e8c81ada..1111cf090a 100644
--- a/src/crawlee/http_clients/_impit.py
+++ b/src/crawlee/http_clients/_impit.py
@@ -4,6 +4,7 @@
 from contextlib import asynccontextmanager
 from logging import getLogger
 from typing import TYPE_CHECKING, Any, TypedDict
+from urllib.request import Request as UrllibRequest
 
 from cachetools import LRUCache
 from impit import AsyncClient, Browser, HTTPError, Response, TimeoutException, TransportError
@@ -30,6 +31,9 @@
 
 logger = getLogger(__name__)
 
+# Cache key: (proxy_url, id(cookie_jar) or None)
+_ClientCacheKey = tuple[str | None, int | None]
+
 
 class _ClientCacheEntry(TypedDict):
     """Type definition for client cache entries."""
@@ -116,7 +120,42 @@ def __init__(
 
         self._async_client_kwargs = async_client_kwargs
 
-        self._client_by_proxy_url = LRUCache[str | None, _ClientCacheEntry](maxsize=10)
+        self._client_cache = LRUCache[_ClientCacheKey, _ClientCacheEntry](maxsize=10)
+
+    def _prepare_cookies_and_headers(
+        self,
+        *,
+        session: Session | None,
+        url: str,
+        headers: HttpHeaders | dict[str, str] | None,
+    ) -> tuple[CookieJar | None, HttpHeaders]:
+        """Resolve cookie jar / Cookie header based on `persist_cookies_per_session`.
+
+        When persistence is enabled, attach the session jar to Impit so response cookies update it.
+        When persistence is disabled, send existing cookies via the `Cookie` header and keep the
+        shared client (no jar) so clients stay cached and reusable.
+        """
+        if isinstance(headers, dict) or headers is None:
+            headers = HttpHeaders(headers or {})
+
+        if session is None:
+            return None, headers
+
+        if self._persist_cookies_per_session:
+            return session.cookies.jar, headers
+
+        if cookie_header := self._get_cookie_header(session.cookies.jar, url, headers):
+            headers = headers | HttpHeaders({'Cookie': cookie_header})
+
+        return None, headers
+
+    @staticmethod
+    def _get_cookie_header(jar: CookieJar, url: str, headers: HttpHeaders | None = None) -> str:
+        """Build a Cookie request header from a jar without attaching the jar to the client."""
+        # UrllibRequest is only used to format Cookie headers via CookieJar; it never opens a connection.
+        request = UrllibRequest(url, headers=dict(headers) if headers else {})  # noqa: S310
+        jar.add_cookie_header(request)
+        return request.get_header('Cookie', '')
 
     @override
     async def crawl(
@@ -128,14 +167,19 @@ async def crawl(
         statistics: Statistics | None = None,
         timeout: timedelta | None = None,
     ) -> HttpCrawlingResult:
-        client = self._get_client(proxy_info.url if proxy_info else None, session.cookies.jar if session else None)
+        cookie_jar, headers = self._prepare_cookies_and_headers(
+            session=session,
+            url=request.url,
+            headers=request.headers,
+        )
+        client = self._get_client(proxy_info.url if proxy_info else None, cookie_jar)
 
         try:
             response = await client.request(
                 url=request.url,
                 method=request.method,
                 content=request.payload,
-                headers=dict(request.headers) if request.headers else None,
+                headers=dict(headers) if headers else None,
                 timeout=timeout.total_seconds() if timeout else None,
             )
         except TimeoutException as exc:
@@ -166,10 +210,8 @@ async def send_request(
     ) -> HttpResponse:
         validate_http_url(url)
 
-        if isinstance(headers, dict) or headers is None:
-            headers = HttpHeaders(headers or {})
-
-        client = self._get_client(proxy_info.url if proxy_info else None, session.cookies.jar if session else None)
+        cookie_jar, headers = self._prepare_cookies_and_headers(session=session, url=url, headers=headers)
+        client = self._get_client(proxy_info.url if proxy_info else None, cookie_jar)
 
         try:
             response = await client.request(
@@ -203,7 +245,8 @@ async def stream(
     ) -> AsyncGenerator[HttpResponse]:
         validate_http_url(url)
 
-        client = self._get_client(proxy_info.url if proxy_info else None, session.cookies.jar if session else None)
+        cookie_jar, headers = self._prepare_cookies_and_headers(session=session, url=url, headers=headers)
+        client = self._get_client(proxy_info.url if proxy_info else None, cookie_jar)
 
         try:
             response = await client.request(
@@ -222,18 +265,22 @@ async def stream(
         finally:
             response.close()
 
+    @staticmethod
+    def _make_cache_key(proxy_url: str | None, cookie_jar: CookieJar | None) -> _ClientCacheKey:
+        return (proxy_url, id(cookie_jar) if cookie_jar is not None else None)
+
     def _get_client(self, proxy_url: str | None, cookie_jar: CookieJar | None) -> AsyncClient:
-        """Retrieve or create an HTTP client for the given proxy URL.
+        """Retrieve or create an HTTP client for the given proxy URL and cookie jar.
 
-        If a client for the specified proxy URL does not exist, create and store a new one.
+        Clients are cached by `(proxy_url, cookie_jar identity)` so sessions with different jars do not share
+        a client. When cookie persistence is disabled, cookies are sent via headers and `cookie_jar` is `None`,
+        so a shared client can be reused for the proxy.
         """
-        cached_data = self._client_by_proxy_url.get(proxy_url)
-        if cached_data:
-            client = cached_data['client']
-            client_cookie_jar = cached_data['cookie_jar']
-            if client_cookie_jar is cookie_jar:
-                # If the cookie jar matches, return the existing client.
-                return client
+        cache_key = self._make_cache_key(proxy_url, cookie_jar)
+
+        cached_data = self._client_cache.get(cache_key)
+        if cached_data and cached_data['cookie_jar'] is cookie_jar:
+            return cached_data['client']
 
         # Prepare a default kwargs for the new client.
         kwargs: dict[str, Any] = {
@@ -249,7 +296,7 @@ def _get_client(self, proxy_url: str | None, cookie_jar: CookieJar | None) -> As
 
         client = AsyncClient(**kwargs, cookie_jar=cookie_jar)
 
-        self._client_by_proxy_url[proxy_url] = _ClientCacheEntry(client=client, cookie_jar=cookie_jar)
+        self._client_cache[cache_key] = _ClientCacheEntry(client=client, cookie_jar=cookie_jar)
 
         return client
 
@@ -270,4 +317,4 @@ def _is_proxy_error(error: HTTPError) -> bool:
     @override
     async def cleanup(self) -> None:
         """Clean up resources used by the HTTP client."""
-        self._client_by_proxy_url.clear()
+        self._client_cache.clear()
diff --git a/tests/unit/http_clients/test_http_clients.py b/tests/unit/http_clients/test_http_clients.py
index aa95e1f62e..592c0eb5ae 100644
--- a/tests/unit/http_clients/test_http_clients.py
+++ b/tests/unit/http_clients/test_http_clients.py
@@ -2,6 +2,7 @@
 
 import asyncio
 import importlib
+import json
 import os
 import sys
 from typing import TYPE_CHECKING
@@ -14,6 +15,7 @@
 from crawlee import Request
 from crawlee.errors import ProxyError
 from crawlee.http_clients import CurlImpersonateHttpClient, HttpClient, HttpxHttpClient, ImpitHttpClient
+from crawlee.sessions import Session
 from crawlee.statistics import Statistics
 from tests.unit.server import generate_file_content
 from tests.unit.server_endpoints import HELLO_WORLD
@@ -323,3 +325,65 @@ def test_import_error_handled(optional_module_name: str, import_path: str) -> No
                 sys.modules.pop(mod_name, None)
         with pytest.raises(ImportError):
             importlib.import_module(import_path)
+
+
+async def test_send_request_sends_session_cookies(http_client: HttpClient, server_url: URL) -> None:
+    """`send_request` must attach existing session cookies (same as `crawl`)."""
+    session = Session()
+    session.cookies.set('auth', 'token-1', domain=server_url.host or '127.0.0.1', path='/')
+
+    response = await http_client.send_request(str(server_url / 'cookies'), session=session)
+    body = json.loads(await response.read())
+
+    assert body['cookies'] == {'auth': 'token-1'}
+
+
+async def test_stream_sends_session_cookies(http_client: HttpClient, server_url: URL) -> None:
+    """`stream` must attach existing session cookies (same as `crawl`)."""
+    session = Session()
+    session.cookies.set('auth', 'token-2', domain=server_url.host or '127.0.0.1', path='/')
+
+    content = b''
+    async with http_client.stream(str(server_url / 'cookies'), session=session) as response:
+        async for chunk in response.read_stream():
+            content += chunk
+
+    assert json.loads(content)['cookies'] == {'auth': 'token-2'}
+
+
+@pytest.mark.parametrize(
+    'custom_http_client',
+    [
+        pytest.param(CurlImpersonateHttpClient(persist_cookies_per_session=False), id='curl'),
+        pytest.param(HttpxHttpClient(persist_cookies_per_session=False), id='httpx'),
+        pytest.param(ImpitHttpClient(persist_cookies_per_session=False), id='impit'),
+    ],
+    indirect=['custom_http_client'],
+)
+async def test_persist_cookies_per_session_false(custom_http_client: HttpClient, server_url: URL) -> None:
+    """When persistence is disabled, response Set-Cookie must not update the session jar."""
+    session = Session()
+    request = Request.from_url(str(server_url.with_path('set_cookies').extend_query(a=1)))
+
+    await custom_http_client.crawl(request, session=session)
+
+    assert {cookie['name']: cookie['value'] for cookie in session.cookies.get_cookies_as_dicts()} == {}
+
+
+@pytest.mark.parametrize(
+    'custom_http_client',
+    [
+        pytest.param(CurlImpersonateHttpClient(persist_cookies_per_session=True), id='curl'),
+        pytest.param(HttpxHttpClient(persist_cookies_per_session=True), id='httpx'),
+        pytest.param(ImpitHttpClient(persist_cookies_per_session=True), id='impit'),
+    ],
+    indirect=['custom_http_client'],
+)
+async def test_persist_cookies_per_session_true(custom_http_client: HttpClient, server_url: URL) -> None:
+    """When persistence is enabled, response Set-Cookie must update the session jar."""
+    session = Session()
+    request = Request.from_url(str(server_url.with_path('set_cookies').extend_query(a=1)))
+
+    await custom_http_client.crawl(request, session=session)
+
+    assert {cookie['name']: cookie['value'] for cookie in session.cookies.get_cookies_as_dicts()} == {'a': '1'}
diff --git a/tests/unit/http_clients/test_httpx.py b/tests/unit/http_clients/test_httpx.py
index c98ca4bbf7..b0a97d8755 100644
--- a/tests/unit/http_clients/test_httpx.py
+++ b/tests/unit/http_clients/test_httpx.py
@@ -3,9 +3,12 @@
 import json
 import logging
 from typing import TYPE_CHECKING
+from unittest.mock import patch
 
 import pytest
 
+from crawlee._types import HttpHeaders
+from crawlee.fingerprint_suite import HeaderGenerator
 from crawlee.fingerprint_suite._browserforge_adapter import get_available_header_values
 from crawlee.fingerprint_suite._consts import COMMON_ACCEPT_LANGUAGE
 from crawlee.http_clients import HttpxHttpClient
@@ -54,3 +57,19 @@ async def test_common_headers_and_user_agent(server_url: URL, header_network: di
     assert 'user-agent' in response_headers
     assert 'python-httpx' not in response_headers['user-agent']
     assert response_headers['user-agent'] in get_available_header_values(header_network, {'User-Agent', 'user-agent'})
+
+
+async def test_headers_come_from_single_fingerprint() -> None:
+    """Accept and User-Agent must come from the same generated fingerprint profile."""
+    header_generator = HeaderGenerator()
+    fingerprint = {'Accept': 'text/html', 'Accept-Language': 'en-US', 'User-Agent': 'TestAgent/1.0'}
+
+    with patch.object(header_generator, 'get_specific_headers', return_value=HttpHeaders(fingerprint)) as mocked:
+        client = HttpxHttpClient(header_generator=header_generator)
+        combined = client._combine_headers(None)
+
+    mocked.assert_called_once_with(header_names={'Accept', 'Accept-Language', 'User-Agent'})
+    assert combined is not None
+    assert combined['accept'] == 'text/html'
+    assert combined['accept-language'] == 'en-US'
+    assert combined['user-agent'] == 'TestAgent/1.0'
diff --git a/tests/unit/http_clients/test_impit.py b/tests/unit/http_clients/test_impit.py
new file mode 100644
index 0000000000..08cd577a02
--- /dev/null
+++ b/tests/unit/http_clients/test_impit.py
@@ -0,0 +1,25 @@
+from __future__ import annotations
+
+from typing import TYPE_CHECKING
+
+from crawlee.http_clients import ImpitHttpClient
+
+if TYPE_CHECKING:
+    from yarl import URL
+
+
+async def test_cleanup_clears_client_cache(server_url: URL) -> None:
+    """`ImpitHttpClient.cleanup` must drop cached clients so the next request creates a fresh one."""
+    client = ImpitHttpClient()
+    async with client:
+        await client.send_request(str(server_url))
+        assert len(client._client_cache) == 1
+        first_client = next(iter(client._client_cache.values()))['client']
+
+        await client.cleanup()
+        assert len(client._client_cache) == 0
+
+        await client.send_request(str(server_url))
+        assert len(client._client_cache) == 1
+        second_client = next(iter(client._client_cache.values()))['client']
+        assert second_client is not first_client