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.
The airfield contracted after the war, and much evidence of this is visible in farmland surrounding the current perimeter. During the 1950s RAF Oakington was an Advanced Flying Training School (No. 5 FTS), converting trainee pilots to jets on Vampires and in the 1960s and 1970s it was used for flight training, operating Vickers Varsity aircraft. When the need for training on piston engined aircraft reduced it was closed, becoming a British Armybarracks.
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.