The airfield was established in the suburb of Parap to act as the Australian Terminal as part of the 1919 England to Australia air race. The airfield operated as a combined airfield (a civilian field and a military field).
The Royal Australian Air Force (RAAF) sent No. 12 Squadron RAAF at the aerodrome in September 1939 after the declaration of war against Germany and in increasingly suspicion of Japanese imperialism. By early 1942, the aerodrome was mainly used by the RAAF, although Guinea Airways retained a civilian presence.
The Japanese bombed the aerodrome in a number of raids on Darwin during 1942 resulting in extensive damage to the town and hangar. The hangar was extensively damaged after suffering a direct hit and the damage can still be seen in the north-east corner fabric of the original steel frame. No. 34 Squadron RAAF was formed on 23 February 1942 at the aerodrome.
In 1945 the Department of Aviation made RAAF Darwin available for shared civil aviation purposes and became Darwin International Airport and as a result, the civilian airport at Parap was closed down by the end of 1946.
The main runway was in the location of Ross Smith Avenue, in the suburb of Parap.
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