Formed on land reclaimed from the Waihopai/New River Estuary in 1938, the airport was prone to flooding, notably in 1984 when it was inoperable for two months.

The Invercargill City Council considered moving the airport back to Dawson Farm, Myross Bush, the original site up to 1942.

The site was chosen as it is closer to the city than the original aerodrome, Dawson Farm, located a then considerable 10 km away northeast of Invercargill.

By then World War Two had begun and the RNZAF used it as an auxiliary field while Dawson Farm remained the air force's aerodrome of choice as heavier patrol bombers could land there.

The passenger terminal facilities originally developed around a striking "Festival of Britain" styled two-level structure built in 1963, which featured a distinctive lozenge-shaped roof and fully glazed airside walls giving great views of the runway from the upper deck.

After Air New Zealand removed its jetway in 2012, it was decided to look at refurbishing the ground floor and extending it, or replace the structure which had to be brought up to new Earthquake safety codes.

[6] Though a turboprop aircraft similar in size to the Viscount, it allowed a higher frequency of departure choices up to eight every weekday including late evenings.

Air New Zealand resisted local pressure not to remove the jets, convincing Southlanders that the smaller ATR (and later, Q300 ) aircraft would allow for a higher frequency of service with minimal time difference.

This has involved completely fencing in the airport perimeter, upgrading the rescue truck fleet, installing a screening area for departing passengers using jet services as well as x-ray machines for baggage.

Runway resurfacing with a fresh top of asphalt over its older sections in 2011 has helped to increase weight limits for aircraft usage.

This service is used to transfer medical staff on a daily basis and have seats when available for purchase by the general public via their web site.

Invercargill Airport has had aspirations from the 1980s through to the 2000s as an international destination with proposals that have failed to get off the ground with nearby Queenstown being developed as a more direct route for jet aircraft.

Nonetheless, Invercargill is now used as a fill-up point for international services as well as designated weather diversion airport for flights to and from Queenstown thanks to its longer runway.

Since July 2012, Air New Zealand had used Invercargill as a technical stop when conditions in Queenstown restrict aircraft from taking off with sufficient fuel to fly directly to Australia due to inclement weather or operational reasons (e.g. high payload).

[11] On 3 March 2013, Invercargill handled over 400 passengers on international flights that were diverted from Queenstown due to low cloud[12] while on 17 June 2024, Virgin Australia Flight 148, a Boeing 737-800 service from Queenstown to Melbourne, was diverted to Invercargill after one of the engines stalled from a bird strike while taking off from the former airport.

After the runway was lengthened and paved, larger aircraft such as the C-124 Globemaster, and C-121 Constellation used the airport for emergency and technical stopovers.

[14] Today the airport is visited by aircraft of the United States ANG, Australian RAAF, Italy's Aeronautica Militare and RNZAF as part of Antarctic flight diversion training.

[10] The largest aircraft to regularly land at Invercargill is the Boeing C-17 Globemaster, although the runway has been "buzzed" by USAF KC-10 Extenders, Lockheed C-141 Starlifters and C-5 Galaxy for emergency diversion practise.