The airport was opened in 1963 on land reclaimed from the Firth of Tay. The first scheduled air service began on 5 July 1966, with a service to Glasgow. A fortnight later a feeder service was added for Edinburgh and Prestwick.
The grass runway was replaced by a 1,100 m (3,609 ft) long tarmac runway in the 1970s, and extended to the current length of 1,400 m (4,593 ft) in the 1990s. During the 1980s Air Ecosse operated services to Aberdeen, Carlisle, Manchester, and Esbjerg using Short 330 and Short 360 aircraft.
After the departure of Business Air, the airport was left without any scheduled services for almost a year until April 1999 - 2007, when ScotAirways introduced flights to London City Airport. On 3 March 2008, Loganair announced that it would recommence the routes that had been operated by FlyWhoosh in May 2008, under the new Flybe franchise.
January 2014, HIAL announced that Loganair with its Flybe franchise would take over from City Jet and commence twice-daily flights to London Stansted, once the London City route had withdrawn in March 2014 by City Jet.
RWY 09: 108.1
ADN (ABERDEEN): 114.30
LSM (LOSSIEMOUTH): 111.30
LUK (LEUCHARS): 110.50