Farmland to the east of Hunsdon was requisitioned by the Air Ministry in 1939 to provide for additional fighter air defence of London. Construction began on 9 October 1940 and involved removal of significant areas of woodland and field boundaries, as well as the Old Turkey Cock pub and a number of cottages in Acorn Street. Built initially as a satellite landing field for nearby RAF North Weald, Hunsdon Airfield opened on 4 May 1941. The runways, perimeter track and aircraft hardstands were constructed by George Wimpey & Sons Ltd with most of the buildings built by HJ Janes of Luton. It soon became a significant airfield in its own right for the fledgling night-fighter squadrons of the Royal Air Force.

The role of the early squadrons was the night fighter defence of London & the South-East, including use of the not terribly successful "Turbinlite" system. The airfield was home to 85 Squadron and its charismatic leader, Group Captain Peter Townsend (in later years linked romantically to Princess Margaret), flying black painted Hawker Hurricanes in the early part of 1941 as a night fighter squadron. After successfully playing a role in the Battle Of Britain, the Squadron reverted to the nightfighter role, initially guided by Ground Control Intercept (GCI).

85 Squadron briefly operated the Boulton-Paul Defiant and the twin-engined Douglas Havoc - these aircraft were built in the US for the French Air Force, but diverted to England after France capitulated. 85 Squadron later enjoyed significant success operating the de Havilland Mosquito before moving to West Malling. No. 3 (F) Squadron, one of the oldest Squadrons formed in the RAF, shared Hunsdon with 85 Squadron for a short period operating Hawker Hurricanes then Hawker Typhoons.

Several aircraft types operated from Hunsdon, but by far the most numerous were the Mosquito's of the Royal Canadian Air Force, initially as Nightfighter squadrons and then on "Intruder" operations. This type of operation involved aircraft to orbit at a small distance, from known German nightfighter airfields on the continent, and then engage enemy aircraft as they either took off, or landed. The RCAF squadrons were also involved in the defence of Southern England against the V1 flying bomb menace, with 418 Sqdn having destroyed a staggering eighty two V1 flying bombs and 409 Sqdn a further ten. The De-Havilland Mosquito became the mainstay of the airfield's fighter bomber role and contributed to many significant attacks during the period before and during D-Day. Operation Jericho - the precision bombing raid on Amiens Prison to release French Resistance fighters on the eve of their execution - was flown from Hunsdon on 18 February 1944.

The main runway at Hunsdon was orientated East /West on 270°/090 °. The secondary runway NNE/SSW, was aligned on 210°/030°. The main runway length was originally 1,450 yards long, but, extended by a further 300 yards to the east to a total length of 1,750 yards. The secondary runway was also extended by 200 yards to the South, to a total length of 1,450 yards. Both runways were 50 yards wide and linked by a 40 ft perimeter track. Drem lighting and an angle of approach indicator system was installed to support night flying.

There were eight seperate sites that made up the entire airfield site of Hunsdon. No 1, to No 8, were technical or living accomodation sites, and were to the West of the flying field. The original airfield plans lists sites 1 to 8, each containing around 20 to 33 or so buildings, mostly Temporary Brick, Thornycroft, and Nissen hutting, but hardly any trace of these dispersed sites remain. These buildings housed the camp cinema (350 seats), canteens, ablution blocks, motor transport sheds, and road fuel storage compounds.

The other sites contained the NCO barracks, Officers quarters, and the WAAF living area. The main Officers Mess was located at the large country house of "Bonningtons". The DF station was to the West of the field , with the VHF station to the North. A seperate sewage works, with four buildings, was also included within the sites.

Aircraft hangers were of the blister type, of which there were 16 placed around the perimeter tracks, with one large Bellman hanger in the main technical site on the Northern side of the flying field. The runways were concrete with ashphalt topping. In total there were 448 individual huts and buildings that made up the airfield, but the only extant buildings are the underground battle headquarters, parachute and ammunition stores, air raid shelters and the defensive pillboxes.

At its height more than 2000 personnel were stationed at RAF Hunsdon, and the lives of the service personnel and of village residents became wholly entwined. Operations from Hunsdon ceased within days of VE Day in May 1945, although it was used to receive personnel and materiel returning from Europe until June 1946. Post war it was returned to agriculture, passing through a number of landowners up until its present owners, Ropemaker Properties Limited, the property investment arm of the BP Pension Fund.