The airport is on land formerly owned by Samuel Steele (brother of William Steele, who brought militia-settlers from Sydney to Hamilton in 1864) from about 1880. By 1929 there was a landing ground on the farm, though a site close to the city was also considered. In 1935 Steele's aerodrome was sold for expansion into an airport and opened by the mayor on 12 October. As the world prepared for war, it became clear that a landing strip needed to be constructed in the Hamilton area. By 1935, the air strip was already in service, as a stopover for military aircraft that would land after a long journey. Services provided refueling as well as food and rest for the incoming pilots. Travel by air began to blossom soon after the war was over, and, in 1950, the airport received its first commercial flight. The main runway was sealed in 1965, and turboprop flights began to Hamilton that year, with NAC's Fokker Friendship aircraft operating. The runway was further lengthened to accommodate Vickers Viscount, 1970, and ultimately Boeing 737 aircraft types in 1975. In 1989, the New Zealand government sold the airport to councils representing Hamilton City (50 per cent), Waikato District (15.625 per cent), Waipa District (15.625 per cent), Matamata-Piako District (15.625 per cent) and ?torohanga District (3.125 per cent). This development led to unprecedented growth for the airport. Ansett New Zealand built an independent passenger terminal to the south of the main building, equipping it with a Golden Wing Club lounge and food vending machines. The airline's Ansett NZ division operated flights to Wellington from Hamilton from 1995 until 2000, when Ansett NZ was sold to a New Zealand business consortium and rebranded Qantas NZ, with their own New Zealand domestic flights division. Qantas NZ operated at the airport until 2001, when it went into receivership. The terminal was then occupied by Origin Pacific airlines. This airline operated domestic services until it too went bankrupt in 2006. The small terminal was then left unused. In 1998, Hamilton Airport Motor Inn was developed to cater for travellers using the airport. It was purchased by the airport company in 2019 and is operated as JetPark Hotel Hamilton Airport & Conference Centre. A NZ$15.3 million terminal expansion begun in 2005 featured a 60 per cent increase in floorspace with improved baggage handling areas, better international and domestic check-in space, and passenger security screening. It was completed in late 2007. Hugh McCarroll was the airport's chief executive from the early 2000s until retirement in February 2006. The current chief executive is Mark Morgan. In 1994, the airport became a terminal for trans-Tasman air routes, with charter flights provided on Boeing 727s by Kiwi Travel International Airlines (not to be confused with the United States–based Kiwi International Air Lines) which served Brisbane, Sydney and Melbourne. New Zealand's Kiwi went bankrupt in 1996, but by that time Freedom Air had begun flying the same routes and a route to the Gold Coast with Boeing 737 and aircraft. They also, briefly, operated flights to Nadi, Fiji, in 2005. Freedom Air ultimately decided to make Hamilton International Airport their company hub until parent company Air New Zealand closed the airline down on 30 March 2008 operating its own full service instead. By then, the Airbus A320 was being operated. When passenger numbers dropped to an unsustainable level in August 2009, Air New Zealand ceased services from Hamilton to Australia. However by that time Virgin Australia operated flights from Hamilton with thrice-weekly Boeing 737-800 flights to Brisbane and Sydney; however, passenger numbers remained low and Virgin Australia ended flights on 27 October 2012. In 2024 Jetstar announced that it would serve Hamilton from Sydney and the Gold Coast using their Airbus A320 aircraft from June 2025.