The end of World War II saw the closure of the base, and its conversion to civil use attracted regional and international passenger services with connections to major Canadian cities and seasonal destinations in the United States, the Caribbean and Mexico.

Regular services to the United States declined as nearby Buffalo Niagara International Airport gained popularity for cross-border travellers in the region, but Hamilton remained an important base for a number of domestic low-cost carriers.

During World War II, the field hosted two units for the British Commonwealth Air Training Plan: first, No.

10 Elementary Flying Training School (later moved to RCAF Station Pendleton) using the De Havilland Tiger Moth and Fleet Finch, then No.

After the war, the airport gradually shifted towards civil use, until the military ceased using it as a base for Air Reserve operations in 1964.

In April 2004, seeking to compete with Air Canada for business travellers, WestJet moved its eastern hub from Hamilton to Toronto Pearson International Airport.

Citing high fuel prices, Air Canada Jazz withdrew its services from Hamilton airport to Montreal and Ottawa by 2008.

[9] In 2015, Air Canada Rouge planned to begin daily service to Calgary by June 2015 but the launch was delayed and ultimately cancelled.

In 2018, ultra-low-cost carriers including Swoop, Flair Airlines, Canada Jetlines chose Hamilton as a hub for service to the Greater Toronto region.

Flair Airlines later shifted operations to Toronto-Pearson in mid-2018 and Air Canada Express again ended its service to Montreal in early-2019.

[16] During the COVID-19 pandemic in Ontario, Hamilton airport saw 60% reduction in passenger services over the year 2020 while peak levels of cargo operations were maintained.

[17] The airport was a key entry point for imported medical supplies into the country, including Canada's first shipment of the Pfizer–BioNTech vaccine which landed on December 14, 2020 from Cologne, Germany by UPS Airlines.

[18] In January 2023, Icelandic airline Play announced plans to bring flights between Hamilton and Reykjavík in June 2023,[19] re-introducing service to Europe.

[21] Hamilton charges 30 to 50 per cent lower fees to airlines than Pearson and its compact size makes travel quicker for passengers and allows aircraft to spend less time on the ground.

[33][34] Megabus began daily express service between the airport and Toronto in 2019,[35] as of 2024 serving one trip a day from the Union Station Bus Terminal.