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No.1 flight was formed in January 1946. The Squadron did not have its own facilities and held lectures at the Teachers' Training College on Barton Terrace, North Adelaide.
During 1948 the flight moved to Keswick Barracks and soon after, formed the first Squadron Band. Both No.1 Flight and the Squadron Band then moved back to the South Australian Headquarters.
In 1987 the flight moved to Croydon High School with No.11 Flight. Two years later both flights merged to become No.1 Flight, Croydon. A few years later the flight moved to a shed in Keswick Barracks.
In 2001, No.1 Flight moved to its current building and soon after was renamed 601 Squadron, the South Australian Squadron was renamed No.6 Wing and the Air Training Corps (ATC) was renamed the Australian Air Force Cadets (AAFC).