diff --git a/CHANGELOG.md b/CHANGELOG.md
index 9c4e2c3875..be1c1707a9 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -6,6 +6,10 @@
 
 - (snapshots) Compress preprod snapshot manifest with zstd ([#3336](https://github.com/getsentry/sentry-cli/pull/3336))
 
+### Fixes
+
+- (auth) Route org token requests to region_url ([#3342](https://github.com/getsentry/sentry-cli/pull/3342))
+
 ## 3.5.1
 
 ### Internal Changes 🔧
diff --git a/src/config.rs b/src/config.rs
index 30296962dd..52ecf847b1 100644
--- a/src/config.rs
+++ b/src/config.rs
@@ -75,7 +75,7 @@ impl Config {
         let manually_configured_url = configured_url(&ini);
         let token_url = token_embedded_data
             .as_ref()
-            .map(|td| td.url.as_str())
+            .map(|td| td.base_url())
             .unwrap_or_default();
 
         let url = if token_url.is_empty() {
@@ -201,7 +201,7 @@ impl Config {
             Some(Auth::Token(ref val)) => {
                 self.cached_token_data = val.payload().cloned();
 
-                if let Some(token_url) = self.cached_token_data.as_ref().map(|td| td.url.as_str()) {
+                if let Some(token_url) = self.cached_token_data.as_ref().map(|td| td.base_url()) {
                     self.cached_base_url = token_url.to_owned();
                 }
 
@@ -232,7 +232,7 @@ impl Config {
         let token_url = self
             .cached_token_data
             .as_ref()
-            .map(|td| td.url.as_str())
+            .map(|td| td.base_url())
             .unwrap_or_default();
 
         if !token_url.is_empty() && url != token_url {
diff --git a/src/utils/auth_token/org_auth_token.rs b/src/utils/auth_token/org_auth_token.rs
index c464a2d0cf..b2997109b4 100644
--- a/src/utils/auth_token/org_auth_token.rs
+++ b/src/utils/auth_token/org_auth_token.rs
@@ -19,6 +19,23 @@ pub struct AuthTokenPayload {
     // URL may be missing from some old auth tokens, see getsentry/sentry#57123
     #[serde(deserialize_with = "url_deserializer")]
     pub url: String,
+
+    // Region URL is the host that actually serves this org's API requests. It is
+    // absent from older tokens, in which case requests fall back to `url`.
+    #[serde(default, deserialize_with = "url_deserializer")]
+    pub region_url: String,
+}
+
+impl AuthTokenPayload {
+    /// Returns the base URL that API requests for this org should target,
+    /// preferring the region URL and falling back to `url` when it is absent.
+    pub fn base_url(&self) -> &str {
+        if self.region_url.is_empty() {
+            &self.url
+        } else {
+            &self.region_url
+        }
+    }
 }
 
 /// Deserializes a URL from a string, returning an empty string if the URL is missing or null.
diff --git a/src/utils/auth_token/test.rs b/src/utils/auth_token/test.rs
index a25568b150..52e452fd59 100644
--- a/src/utils/auth_token/test.rs
+++ b/src/utils/auth_token/test.rs
@@ -21,12 +21,54 @@ fn test_valid_org_auth_token() {
     let payload = token.payload().unwrap();
     assert_eq!(payload.org, "sentry");
     assert_eq!(payload.url, "http://localhost:8000");
+    assert_eq!(payload.region_url, "http://localhost:8000");
+    assert_eq!(payload.base_url(), "http://localhost:8000");
 
     assert_eq!(good_token, token.raw().expose_secret().clone());
 
     assert!(token.format_recognized());
 }
 
+#[test]
+fn test_valid_org_auth_token_region_url_differs() {
+    // Payload: {"url":"http://control.example","region_url":"http://region.example","org":"sentry"}
+    let good_token = String::from(
+        "sntrys_\
+            eyJpYXQiOiAxNzA0MjA1ODAyLjE5OTc0MywgInVybCI6ICJodHRwOi8vY29udHJvbC5leGFtcGxlIiw\
+            gInJlZ2lvbl91cmwiOiAiaHR0cDovL3JlZ2lvbi5leGFtcGxlIiwgIm9yZyI6ICJzZW50cnkifQ==_\
+            lQ5ETt61cHhvJa35fxvxARsDXeVrd0pu4/smF4sRieA",
+    );
+
+    let token = AuthToken::from(good_token);
+    let payload = token.payload().unwrap();
+
+    assert_eq!(payload.org, "sentry");
+    assert_eq!(payload.url, "http://control.example");
+    assert_eq!(payload.region_url, "http://region.example");
+    // base_url prefers region_url when present.
+    assert_eq!(payload.base_url(), "http://region.example");
+}
+
+#[test]
+fn test_valid_org_auth_token_missing_region_url() {
+    // Legacy token with no region_url field at all; base_url falls back to url.
+    // Payload: {"url":"http://legacy.example","org":"sentry"}
+    let good_token = String::from(
+        "sntrys_\
+            eyJpYXQiOiAxNzA0MjA1ODAyLjE5OTc0MywgInVybCI6ICJodHRwOi8vbGVnYWN5LmV4YW1wbGUiL\
+            CAib3JnIjogInNlbnRyeSJ9_\
+            lQ5ETt61cHhvJa35fxvxARsDXeVrd0pu4/smF4sRieA",
+    );
+
+    let token = AuthToken::from(good_token);
+    let payload = token.payload().unwrap();
+
+    assert_eq!(payload.org, "sentry");
+    assert_eq!(payload.url, "http://legacy.example");
+    assert!(payload.region_url.is_empty());
+    assert_eq!(payload.base_url(), "http://legacy.example");
+}
+
 #[test]
 fn test_valid_org_auth_token_missing_url() {
     let good_token = String::from(
@@ -43,6 +85,9 @@ fn test_valid_org_auth_token_missing_url() {
     let payload = token.payload().unwrap();
     assert_eq!(payload.org, "sentry");
     assert!(payload.url.is_empty());
+    // url is null but region_url is present, so base_url falls back to region_url.
+    assert_eq!(payload.region_url, "http://localhost:8000");
+    assert_eq!(payload.base_url(), "http://localhost:8000");
 
     assert_eq!(good_token, token.raw().expose_secret().clone());
 
diff --git a/tests/integration/_cases/org_tokens/region-url-routing.trycmd b/tests/integration/_cases/org_tokens/region-url-routing.trycmd
new file mode 100644
index 0000000000..f209e9b2ce
--- /dev/null
+++ b/tests/integration/_cases/org_tokens/region-url-routing.trycmd
@@ -0,0 +1,10 @@
+A region-scoped org token where url (control silo) differs from region_url (the org's
+region host). The region_url governs routing: it is preferred over the token's url and
+overrides --url. Payload: {"url":"http://control.example","region_url":"http://region.example","org":"sentry"}
+```
+$ sentry-cli --auth-token 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 --url http://example.com info
+? failed
+[..]WARN[..] Using http://region.example (embedded in token) rather than manually-configured URL http://example.com. To use http://example.com, please provide an auth token for this URL.
+...
+
+```
diff --git a/tests/integration/_cases/org_tokens/url-mismatch-empty-token.trycmd b/tests/integration/_cases/org_tokens/url-mismatch-empty-token.trycmd
index db83846b6c..d95a53240a 100644
--- a/tests/integration/_cases/org_tokens/url-mismatch-empty-token.trycmd
+++ b/tests/integration/_cases/org_tokens/url-mismatch-empty-token.trycmd
@@ -1,8 +1,9 @@
-This auth token has an empty URL. We expect the --url argument to take precedence here
+This token has an empty url but a non-empty region_url. The region_url now governs
+routing, so it overrides the --url argument (the warning references the region_url).
 ```
 $ sentry-cli --auth-token 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 --url https://sentry.example.com info
 ? failed
-Sentry Server: https://sentry.example.com
+[..]WARN[..] Using http://localhost:8000 (embedded in token) rather than manually-configured URL https://sentry.example.com. To use https://sentry.example.com, please provide an auth token for this URL.
 ...
 
 ```