Wakkanai Airport opened to passenger traffic in 1960, initially with a 1200-meter runway, and flights by Japan Domestic Airlines to Okadama Airport on an irregular basis. Japan Domestic Airlines was replaced by Yokohama Airlines in 1965. Air Nippon began scheduled service to Okadama Airport and Rishiri Airport in 1974, followed by Rebun Airport in 1978 and New Chitose Airport in 1980. The city of Wakkanai provided subsidies for city residents to use the flight until 2005, when discounted fares became available. In 1987, the runway was lengthened to 1800 meters and a new terminal building was opened on the south side of the runway to handle jet operations. This allowed All Nippon Airways to begin jet service to Tokyo. The flight was initially seasonal and did not become a year-round service until 1997. The runway was extended again, to 2000 meters in 1988 and an instrument landing system (ILS) was installed. The terminal building was expanded in 1998. Air Hokkaido discontinued the short Rebun and Rishiri commuter flights in 2003 due to poor load factors. The runway was further extended to 2200 meters in 2009. In 2016, air traffic control operations were transferred to New Chitose Airport. The airport was privatized in 2021.

As of 2025, ANA has two scheduled daily round trips to Sapporo using Bombardier Q400 turboprops (operated by ANA Wings), and one scheduled daily round trip to Tokyo (two from June to September) using Boeing 737 and Airbus A321 jets.

On 20 August 2025, an ANA Wings Bombardier Q400 arriving from Sapporo-Chitose nearly collided with a runway vehicle while landing on runway 08/26. The Ministry of Transport categorized the event as a "serious incident" and initiated an investigation.