In 1938, the Fort St. John Board of Trade sponsored the construction of an airport and approached the Department of Transport for financial assistance. The Department of Transport required an airport at Fort St. John as part of the new airway planned between Edmonton and Whitehorse. It purchased a site and constructed a landing strip 4,000 ft (1,219 meters by 122 meters) which was completed in the spring of 1940. When the United States entered the war, the Edmonton to Whitehorse route took on a greater significance and was developed into the Northwest Staging Route to Alaska.

A large construction program was undertaken in 1942 to connect the existing airfields with the Alaska Highway and to provide additional emergency fields and navigation aids between Edmonton and Northway, Alaska. In 1943, American contractors assumed responsibility for the completion of the work at a number of airports, including Fort St. John. The USAF constructed a completely new facility at a location east of the community, which today remains as the location of the Fort St. John Airport. The original airport was closed down in the winter of 1943-44. At the end of the war, Canada bought all the facilities that were constructed by the US. The Fort St. John Airport was taken over by the Department of Transport on April 10, 1951.

Under the National Airports Policy, announced by Transport Canada in 1994, the Fort St. John Airport became eligible for ownership by local interests.

In January of 1997 the North Peace Airport Society signed documents transferring ownership from Transport Canada to the Society. As of March 18, 1997, the airport is operated by North Peace Airport Services Ltd., a wholly owned subsidiary of Vancouver International Airport Authority.