diff --git a/docs/2577.bugfix.rst b/docs/2577.bugfix.rst
new file mode 100644
index 0000000000..ca77d76aca
--- /dev/null
+++ b/docs/2577.bugfix.rst
@@ -0,0 +1 @@
+Changed HTTPSConnection so that ``proxy_ssl_context`` must be set when ``use_forwarding_for_https`` is set to ``True``
\ No newline at end of file
diff --git a/src/urllib3/connection.py b/src/urllib3/connection.py
index d3634e5654..50d115ee77 100644
--- a/src/urllib3/connection.py
+++ b/src/urllib3/connection.py
@@ -421,7 +421,22 @@ def __init__(
         self.key_file = key_file
         self.cert_file = cert_file
         self.key_password = key_password
-        self.ssl_context = ssl_context
+
+        if proxy_config and proxy_config.use_forwarding_for_https and ssl_context:
+            if proxy_config.ssl_context:
+                raise ValueError(
+                    "Parameter ssl_context cannot be set when use_forwarding_for_https is True"
+                )
+            else:
+                raise ValueError(
+                    "Parameter ssl_context cannot be set when use_forwarding_for_https is True. Set parameter proxy_ssl_context instead"
+                )
+
+        self.ssl_context = (
+            proxy_config.ssl_context
+            if proxy_config and proxy_config.use_forwarding_for_https
+            else ssl_context
+        )
         self.server_hostname = server_hostname
         self.ssl_version = None
         self.ssl_minimum_version = None
diff --git a/test/with_dummyserver/test_proxy_poolmanager.py b/test/with_dummyserver/test_proxy_poolmanager.py
index e3994f3f10..4edbdba7e8 100644
--- a/test/with_dummyserver/test_proxy_poolmanager.py
+++ b/test/with_dummyserver/test_proxy_poolmanager.py
@@ -394,6 +394,48 @@ def test_https_headers_forwarding_for_https(self) -> None:
                 returned_headers.get("Host") == f"{self.https_host}:{self.https_port}"
             )
 
+    def test_forwarding_for_https_with_proxy_ctx(self) -> None:
+        proxy_ctx = ssl.create_default_context()
+        proxy_ctx.load_verify_locations(DEFAULT_CA)
+        with proxy_from_url(
+            self.https_proxy_url,
+            headers={"Foo": "bar"},
+            proxy_headers={"Hickory": "dickory"},
+            proxy_ssl_context=proxy_ctx,
+            use_forwarding_for_https=True,
+        ) as http:
+            r = http.request("GET", f"{self.https_url}/")
+            assert r.status == 200
+
+    def test_forwarding_for_https_error_with_ssl_ctx(self) -> None:
+        proxy_ctx = ssl.create_default_context()
+        proxy_ctx.load_verify_locations(DEFAULT_CA)
+        ctx = ssl.create_default_context()
+        ctx.load_verify_locations(DEFAULT_CA)
+        with proxy_from_url(
+            self.https_proxy_url,
+            proxy_ssl_context=proxy_ctx,
+            use_forwarding_for_https=True,
+            ssl_context=ctx,
+        ) as proxy:
+            with pytest.raises(
+                ValueError,
+                match="Parameter ssl_context cannot be set when use_forwarding_for_https is True",
+            ):
+                proxy.request("GET", self.https_url)
+
+    def test_forwarding_for_https_error_with_only_ssl_ctx(self) -> None:
+        ctx = ssl.create_default_context()
+        ctx.load_verify_locations(DEFAULT_CA)
+        with proxy_from_url(
+            self.https_proxy_url, use_forwarding_for_https=True, ssl_context=ctx
+        ) as proxy:
+            with pytest.raises(
+                ValueError,
+                match="Parameter ssl_context cannot be set when use_forwarding_for_https is True. Set parameter proxy_ssl_context instead",
+            ):
+                proxy.request("GET", self.https_url)
+
     def test_headerdict(self) -> None:
         default_headers = HTTPHeaderDict(a="b")
         proxy_headers = HTTPHeaderDict()
@@ -571,19 +613,13 @@ def test_https_proxy_tls_error(
 
     @requires_network()
     @pytest.mark.parametrize(
-        ["proxy_scheme", "use_forwarding_for_https"],
+        ["proxy_scheme"],
         [
-            ("http", False),
-            ("https", False),
-            ("https", True),
+            ("http",),
+            ("https",),
         ],
     )
-    def test_proxy_https_target_tls_error(
-        self, proxy_scheme: str, use_forwarding_for_https: str
-    ) -> None:
-        if proxy_scheme == "https" and use_forwarding_for_https:
-            pytest.skip("Test is expected to fail due to urllib3/urllib3#2577")
-
+    def test_proxy_https_target_tls_error(self, proxy_scheme: str) -> None:
         proxy_url = self.https_proxy_url if proxy_scheme == "https" else self.proxy_url
         proxy_ctx = ssl.create_default_context()
         proxy_ctx.load_verify_locations(DEFAULT_CA)
@@ -593,7 +629,7 @@ def test_proxy_https_target_tls_error(
             proxy_url,
             proxy_ssl_context=proxy_ctx,
             ssl_context=ctx,
-            use_forwarding_for_https=use_forwarding_for_https,
+            use_forwarding_for_https=False,
         ) as proxy:
             with pytest.raises(MaxRetryError) as e:
                 proxy.request("GET", self.https_url)