601 squadron was formed in October 1925 at Northolt as part of the Auxiliary Air Force. Initially it was a light bomber force, but in January 1939 it receieved Blenheims which were replaced with Hurricanes in March 1940. The squadron spent a week in France before returning to Britain to take part in the emerging Battle of Britain.

Following service in the Middle East and North Africa, the squadron was disbanded on 14 August 1945. In June 1946 it was reformed as part of the Auxiliary Air Force. The Auxiliary Air Force was eventually disbanded in 1957 and the squadron was also disbanded.