Queenstown Airport was first licensed to operate in 1935, but it was not until the 1950s that commercial flights became commonplace, particularly commercial sightseeing operations to Milford Sound.

A regular scenic route between Queenstown and Dunedin was first established by Southern Scenic Air Services Ltd on 17 July 1950.

In the 1960s, the original grass runway was lengthened.

Mount Cook Airline was the pioneer of tourist flights into Queenstown.

Regular services from Christchurch began on 6 November 1961, operating DC-3s with three flights a week on a Monday, Wednesday, and Friday to Queenstown via Mount Cook and onto Te Anau-Manapouri.

Ansett New Zealand introduced the first jet aircraft flights into Queenstown Airport in 1989 using British Aerospace 146 aircraft.

In 1995, Air New Zealand began operating Queenstown Airport's first trans-Tasman flight from Sydney. Since this, an almost continuous expansion programme began to cater to passenger and airline demand.

In 2010, runway lighting was installed to enhance low-visibility operations during daytime. In 2012, the airspace around Queenstown was redesigned to allow for Required Navigation Performance, Authorisation Required (RNP AR) operations.

In April 2012, Queenstown Airport opened its new sealed cross-wind runway on the former grass runway; the cost of this project was $800,000 and took 10 months to complete. Sealing the runway reduced the number of disruptions as well as further improved safety."

After announcing plans to expand the airport in 2010, work began in 2014 to extend the international terminal. On 23 June 2015, the new $17 million international terminal was opened. The 4,100 m2 (44,000 sq ft) expansion to the southern end of the terminal building doubled the size of the airport's international operations, and brought a new mezzanine level on top to enable airbridges to be built at a later stage.

In November 2015, Queenstown Airport commenced a $17 million series of major airfield infrastructure improvements designed to improve operations for evening flights in winter 2016 and improve overall safety and efficiency of operations.

In June 2015, the airport launched its new international terminal.

In May 2014, New Zealand's Civil Aviation Authority (CAA) and Australia's Civil Aviation Safety Authority (CASA) approved Queenstown Airport's foundation safety case for after-dark flights, reliant on some additional infrastructure, including upgraded runway lights and widening the main runway to 45 metres (148 ft). On 4 May 2016, the airport's runway lights were officially switched on by transport minister Simon Bridges. The runway lighting allowed the airport to extend operations beyond sunset to its 10:00 pm noise abatement curfew. The first after-dark flight was a Jetstar flight from Melbourne on 24 June 2016.

The airport was voted 'World's Most Scenic Airport Landing' in 2015 by international private jet booking service PrivateFly.

In March 2025, the airport finished installing an engineered materials arrestor system (EMAS) at both ends of the primary runway, becoming the first airport in Australasia to do so. In the event of a runway overrun, this system is designed to safely bring the aircraft to a stop, thus greatly reducing the damage to the aircraft and the risk of injury to those onboard and on the ground.