diff --git a/zulip/zulip/__init__.py b/zulip/zulip/__init__.py
index 82190a51d..c736ece72 100644
--- a/zulip/zulip/__init__.py
+++ b/zulip/zulip/__init__.py
@@ -393,6 +393,7 @@ def __init__(
         config_file: Optional[str] = None,
         verbose: bool = False,
         retry_on_errors: bool = True,
+        auto_retry_rate_limits: bool = False,
         site: Optional[str] = None,
         client: Optional[str] = None,
         cert_bundle: Optional[str] = None,
@@ -476,6 +477,7 @@ def __init__(
         self.api_key = api_key
         self.email = email
         self.verbose = verbose
+        self.auto_retry_rate_limits = auto_retry_rate_limits
         if site is not None:
             if site.startswith("localhost"):
                 site = "http://" + site
@@ -655,6 +657,23 @@ def end_error_retry(succeeded: bool) -> None:
 
                 self.has_connected = True
 
+                # On Rate Limit (429) Errors, pause the current thread with time.sleep()
+                # And only retry if the user opted in sucessfully
+                if res.status_code == 429 and self.auto_retry_rate_limits:
+                    try:
+                        # Zulip will return the wait time in the either the (JSON) body or header
+                        wait_time = float(
+                            res.json().get("retry-after", res.headers.get("Retry-After", 1.0))
+                        )
+                    except Exception:
+                        wait_time = 1.0
+                    if self.verbose:
+                        print(
+                            f"Rate limit hit! Sleeping for {wait_time} seconds before retrying..."
+                        )
+                    time.sleep(wait_time)
+                    continue
+
                 # On 50x errors, try again after a short sleep
                 if str(res.status_code).startswith("5") and error_retry(
                     f" (server {res.status_code})"