[citation needed] By 1935, the air strip was already in service, as a stopover for military aircraft that would land after a long journey.

The main runway was sealed in 1965, and turboprop flights began to Hamilton that year, with NAC's Fokker Friendship aircraft operating.

[11] 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.

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.

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 with Boeing 737 aircraft.

When passenger numbers dropped to an unsustainable level in August 2009, Air New Zealand ceased services from Hamilton to Australia.

The company cited the COVID-19 pandemic as a cause, but not the sole reason[13] The Waikato Aero Club has been based at Hamilton Airport since 1933.

The club provides a full range of flight training from recreational flying in Light Sport Aircraft through to commercial Multi-Engine IFR.

Plans to increase runway length from 2,195m to 3,000m to attract larger aircraft and start Asian regional flights, have been considered.