Known as the 'Civil 'Drome', Cooktown’s first commercial aerodrome was constructed in 1937 to accommodate the DeHavilland Rapide biplanes of Australian National Airways. The airfield was built on an area of level ground at the edge of a coastal mangrove swamp. Due to the area being inundated during most high tides the facility required a long levee bank around its seaward perimeter and extensive flood mitigation measures to contend with rainwater. The areas surrounding the runway still became very soft in the wet season and pilots had to take care not to become bogged.

To assist aircraft using the airfield, Cooktown Aeradio Station was constructed at the civil 'drome by TJ Watkins for the Department of Civil Aviation (DCA), also in 1937. The main station building contained two rooms, one the operating room and the other a store room. The station contained radio telegraphy and morse key equipment, and a compact cathode ray tube used mainly for locating ships. A large bank of receivers was tuned to local frequencies in use. Nearby were the transmission masts and several other buildings containing living and sleeping quarters, and a kitchen and mess.