With the extension of the North Australia Railway in 1926, a bridge across the Katherine River was opened, allowing local businesses to move from the rail head town of Emungalan to more favourable sites on the southern bank of the river in the new township of Katherine. Previously, a rough airstrip built in 1923 had served the area, however with the increased development land was sought and secured in 1930 for a permanent airport 1.5 km (0.93 mi) north-east of the town. In March 1934, Dr Clyde Fenton, newly appointed as Government Medical Officer began operating medical evacuation flights from the airport using a Gipsy Mothbiplane bought with his own money. This operation would lead to the foundation of the Northern Territory Aerial Medical Service. Fenton's aircraft is preserved and on display in a purpose built hangar at the Katherine Museum, adjacent to the former runway. During the 1930s, the airfield was used as a refuelling stop by Guinea Airways, operating flights between Darwin and Adelaide.
The civil airfield was requisitioned by Royal Australian Air Force and the 808th Engineer Aviation Battalion extended the airfield from 19 February 1942 to 13 April 1942. The runway was extended to 5,000 ft (1,524 m) long and 100 feet (30 m) wide and 18 dispersals without revetments were constructed. During 1943, the Department of Civil Aviation established a flight service unit at the airfield which operated until 1978 with the closure of the airfield.
Japanese bombing raids against Katherine Airfield
At 7:50 am on 18 January 1939, a Lockheed Model 14 Super Electra of Guinea Airways (predecessor of Airlines of South Australia) struck trees and crashed into the Katherine River during takeoff from the airfield, killing four on board including three pilots and a Civil Aviation Department inspector. The aircraft was operating a scheduled flight to Adelaide. Dr Clyde Fenton was among the medical responders at the crash site.