Construction was started in 1939, but was affected by the outbreak of war, the original plan called for Type C hangars two type J were erected instead. It was used by No. 2 Group in July 1940 for No. 218 Squadron which had recently returned from France. In September, Oakington was passed on for the No. 2 Group which stationed the first Short StirlingSquadron No. 7. The newly formed No. 3 Photographic Reconnaissance Unit started to use RAF Oakington to conduct high altitude work for Bomber Command's targets however there were poor surface conditions at RAF Oakington so No. 3 PRU often operated from RAF Alconbury.
During the 1950s RAF Oakington was an Advanced Flying Training School, No. 5 Flying Training School, (5 FTS), which reformed at the airfield on 1 June 1954. Its initial role was to convert trainee pilots to jets using De Havilland Vampire T.5 single seat jets and Vampire T.11 twin-seat jets. In March 1962 these types were exchanged for the Vickers Varsity T.1 twin piston-engine navigational trainers. 5 FTS was disbanded on 31 December 1974 when the need for training on piston engined aircraft reduced. The airfield was then closed, becoming a British Armybarracks.
The airfield's land area had contracted after the war, and much evidence of this former military use is visible in farmland surrounding the current perimeter.
Since 2007 plans have been developed to build Northstowe, a new settlement of 9,500 houses on the site. Demolition of parts of the site commenced in late January 2011 by the contractor Sovereign Plant Ltd. Work started on the first 1500 homes and related facilities in 2014.