In 1934, Air Marshal Sir Victor Goddard, then a Wing Commander, was flying over Drem in poor weather. The airfield, at that time disused, was supposed to be derelict: collapsed hangars, weeds in the dispersal pans, no aircraft, no personnel. As he descended through the cloud Goddard saw the airfield as it would look in 1939: rebuilt, freshly painted hangars, mechanics in unfamiliar blue overalls, monoplane fighters in yellow that the RAF did not yet possess. He climbed back into the cloud, and when he came out again, Drem was once more abandoned. Goddard published the account decades later. By then the airfield had indeed been rebuilt, painted in those colours, staffed by men in blue, and stocked with monoplane trainers in a yellow that did not exist in 1934 but did in 1939. The vision is one of the most cited cases in twentieth-century paranormal literature.

The airfield's history pre-dates the RAF. It opened in 1916 as West Fenton Aerodrome, home to 77 Home Defence Squadron of the Royal Flying Corps. In April 1918 the American 41st Aero Squadron arrived under Lieutenant Warren Woodward, calling the airfield Gullane in their official history. By November 1918 it had been renamed Gullane Aerodrome, and with postwar demobilisation it was vacated in 1919. From 1933 to 1939 it saw only occasional use, which was the state Goddard found it in. In 1939 the grass strip was resurfaced and the station was renamed RAF Drem, home to 13 Flying Training School. By the time war was declared in September, 602 Squadron's Spitfires were patrolling from its runways.

Night fighting was a problem nobody had solved when the war started. Pilots could find the enemy in the dark, sometimes, but landing back at base was a different ordeal: an unlit airfield in blackout conditions was nearly invisible from above. In 1940 RAF Drem developed the airfield lighting system that bears its name. The Drem System used a circle of glim lamps marking the airfield boundary, with a funnel of approach lights pointing pilots to the runway threshold, and obstruction lights on hangars and other tall structures. Shielded so that they were invisible from above 1,500 feet but clearly visible to a descending pilot, the lights revolutionized night operations across the RAF and were adopted at airfields throughout the war. The system was a Drem invention, named for the station that solved the problem that every fighter command needed solving.

From 1942 the airfield hosted Royal Naval lodger units, including 784 Night Fighter Training Squadron. On 21 April 1945 the base transferred to the Admiralty as Royal Naval Air Station Drem, commissioned as HMS Nighthawk. Various Fleet Air Arm squadrons used it when disembarking from carriers between 1943 and 1945. In March 1946 the field reverted to RAF control, closed soon after, and was decommissioned. Today equestrian businesses occupy parts of the former dispersals, business premises fill the old accommodation, and a radio-control model aircraft club has a strip along the southern peritrack. The RAF Drem Museum is housed in what was the wartime mess. The station motto, Exiit Hinc Lumen, translates as 'Light has departed from this place,' which feels prescient for a base that invented night landing lights and then quietly went dark itself.