diff --git a/src/sentry/api/endpoints/chunk.py b/src/sentry/api/endpoints/chunk.py
index d0ccb85d0f7e9f..6556ebfe9d9c16 100644
--- a/src/sentry/api/endpoints/chunk.py
+++ b/src/sentry/api/endpoints/chunk.py
@@ -1,4 +1,5 @@
 import logging
+import re
 from gzip import GzipFile
 from io import BytesIO
 from urllib.parse import urljoin
@@ -18,6 +19,7 @@
 MAX_REQUEST_SIZE = 32 * 1024 * 1024
 MAX_CONCURRENCY = settings.DEBUG and 1 or 8
 HASH_ALGORITHM = "sha1"
+SENTRYCLI_SEMVER_RE = re.compile(r"^sentry-cli\/(?P<major>\d+)\.(?P<minor>\d+)\.(?P<patch>\d+).*$")
 
 CHUNK_UPLOAD_ACCEPT = (
     "debug_files",  # DIF assemble
@@ -48,12 +50,29 @@ def get(self, request, organization):
         endpoint = options.get("system.upload-url-prefix")
         relative_url = reverse("sentry-api-0-chunk-upload", args=[organization.slug])
 
+        # Starting `sentry-cli@1.70.1` we added a support for relative chunk-uploads urls
+        # User-Agent: sentry-cli/1.70.1
+        user_agent = request.headers.get("User-Agent", "")
+        sentrycli_version = SENTRYCLI_SEMVER_RE.search(user_agent)
+        supports_relative_url = (
+            (sentrycli_version is not None)
+            and (int(sentrycli_version.group("major")) >= 1)
+            and (int(sentrycli_version.group("minor")) >= 70)
+            and (int(sentrycli_version.group("patch")) >= 1)
+        )
+
+        # If user do not overwritten upload url prefix
         if len(endpoint) == 0:
-            # If config is not set, we return relative, versionless endpoint (with `/api/0` stripped)
-            prefix = "/api/0"
-            url = relative_url.replace(prefix, "/")
+            # And we support relative url uploads, return a relative, versionless endpoint (with `/api/0` stripped)
+            if supports_relative_url:
+                prefix = "/api/0"
+                url = relative_url.replace(prefix, "/")
+            # Otherwise, if we do not support them, return an absolute, versioned endpoint with a default, system-wide prefix
+            else:
+                endpoint = options.get("system.url-prefix")
+                url = urljoin(endpoint.rstrip("/") + "/", relative_url.lstrip("/"))
         else:
-            # Otherwise, we want a relative, versioned endpoint, with user-configured prefix
+            # If user overriden upload url prefix, we want an absolute, versioned endpoint, with user-configured prefix
             url = urljoin(endpoint.rstrip("/") + "/", relative_url.lstrip("/"))
 
         return Response(
diff --git a/tests/sentry/api/endpoints/test_chunk_upload.py b/tests/sentry/api/endpoints/test_chunk_upload.py
index a2f3436506d0ce..030fecf5d60327 100644
--- a/tests/sentry/api/endpoints/test_chunk_upload.py
+++ b/tests/sentry/api/endpoints/test_chunk_upload.py
@@ -1,5 +1,6 @@
 from hashlib import sha1
 
+import pytest
 from django.conf import settings
 from django.core.files.uploadedfile import SimpleUploadedFile
 from django.urls import reverse
@@ -16,6 +17,10 @@
 
 
 class ChunkUploadTest(APITestCase):
+    @pytest.fixture(autouse=True)
+    def _restore_upload_url_options(self):
+        options.delete("system.upload-url-prefix")
+
     def setUp(self):
         self.organization = self.create_organization(owner=self.user)
         self.token = ApiToken.objects.create(user=self.user, scope_list=["project:write"])
@@ -33,7 +38,7 @@ def test_chunk_parameters(self):
         assert response.data["maxFileSize"] == options.get("system.maximum-file-size")
         assert response.data["concurrency"] == MAX_CONCURRENCY
         assert response.data["hashAlgorithm"] == HASH_ALGORITHM
-        assert response.data["url"] == self.url.replace("/api/0", "/")
+        assert response.data["url"] == options.get("system.url-prefix") + self.url
 
         options.set("system.upload-url-prefix", "test")
         response = self.client.get(
@@ -42,6 +47,53 @@ def test_chunk_parameters(self):
 
         assert response.data["url"] == options.get("system.upload-url-prefix") + self.url
 
+    def test_relative_url_support(self):
+        # Starting `sentry-cli@1.70.1` we added a support for relative chunk-uploads urls
+
+        # >= 1.70.1
+        response = self.client.get(
+            self.url,
+            HTTP_AUTHORIZATION=f"Bearer {self.token.token}",
+            HTTP_USER_AGENT="sentry-cli/1.70.1",
+            format="json",
+        )
+        assert response.data["url"] == self.url.replace("/api/0", "/")
+
+        response = self.client.get(
+            self.url,
+            HTTP_AUTHORIZATION=f"Bearer {self.token.token}",
+            HTTP_USER_AGENT="sentry-cli/2.77.4",
+            format="json",
+        )
+        assert response.data["url"] == self.url.replace("/api/0", "/")
+
+        # < 1.70.1
+        response = self.client.get(
+            self.url,
+            HTTP_AUTHORIZATION=f"Bearer {self.token.token}",
+            HTTP_USER_AGENT="sentry-cli/1.70.0",
+            format="json",
+        )
+        assert response.data["url"] == options.get("system.url-prefix") + self.url
+
+        response = self.client.get(
+            self.url,
+            HTTP_AUTHORIZATION=f"Bearer {self.token.token}",
+            HTTP_USER_AGENT="sentry-cli/0.69.3",
+            format="json",
+        )
+        assert response.data["url"] == options.get("system.url-prefix") + self.url
+
+        # user overriden upload url prefix has priority, even when calling from sentry-cli that supports relative urls
+        options.set("system.upload-url-prefix", "test")
+        response = self.client.get(
+            self.url,
+            HTTP_AUTHORIZATION=f"Bearer {self.token.token}",
+            HTTP_USER_AGENT="sentry-cli/1.70.1",
+            format="json",
+        )
+        assert response.data["url"] == options.get("system.upload-url-prefix") + self.url
+
     def test_large_uploads(self):
         with self.feature("organizations:large-debug-files"):
             response = self.client.get(