The airport opened in 1928 as Stevenson Aerodrome in honour of the noted Manitoba aviator and pioneer bush pilot, Captain Fred J. Stevenson. Stevenson Aerodrome, also known as Stevenson Field, was Canada's first international airport with Northwest Airways (which became Northwest Airlines) inaugurating a passenger and mail service between Winnipeg and Pembina, North Dakota on February 2, 1931.

By 1935, Northwest Airlines was operating daily service from the airport with Hamilton H-47 prop aircraft on a routing of Winnipeg – Pembina, ND – Grand Forks – Fargo – Minneapolis/St. Paul, MN – Milwaukee, WI – Chicago, IL.

The City of Winnipeg and the Rural Municipality of St. James agreed to develop Stevenson Field as a modern municipal airport in 1936. In 1938 the Manitoba Legislative Assembly passed the St. James–Winnipeg Airport Commission Act creating a commission of the same name with full control over the operation of the airport. In 1940, during the Second World War, the Government of Canada placed the airport under the direction of the Minister of Transport and the Royal Canadian Air Force where it remained until 1997.

Also in 1940, Trans-Canada Air Lines (TCA) was operating daily round trip transcontinental service across Canada via the airport with a routing of Montreal – Ottawa – North Bay – Kapuskasing – Wagaming – Winnipeg – Regina – Lethbridge – Vancouver flown with Lockheed Model 10 Electra twin prop aircraft with connecting service to and from Toronto being offered via North Bay.

Post-war

In 1962, Stevenson Field was officially renamed Winnipeg International Airport, followed in 1997 by the airport's transfer to the control of the Winnipeg Airports Authority.

The original main terminal building was built in 1964, and was designed by the architectural firm of Green Blankstein Russell and Associates (subsequently GBR Associates and Stantec Limited). It was expanded and renovated in 1984 by the architectural firm of IKOY, and a hotel was built across from the terminal in 1998. The original main terminal building was closed on Sunday October 30, 2011 and has since been demolished.

Winnipeg Airport was briefly served by Scandinavian Airlines (SAS) during the mid-1950s on the world's first regular polar route, which linked Copenhagen and Los Angeles with Douglas DC-6B propliner flights via Søndre Strømfjord, Greenland and Winnipeg.

Two passenger airlines operating jet aircraft were previously based at the Winnipeg International Airport: Transair (Canada) and Greyhound Air (both now-defunct). Transair and Greyhound Air operated scheduled flights across Manitoba, Ontario, the Northwest Territories and the Yukon from its Winnipeg hub in addition to operating charter services from the airport to Europe, the Caribbean, Mexico, Florida, and Hawaii among other destinations in the U.S.

Six airlines were serving the airport with scheduled passenger flights during the 1970s and 1980s. Air Canada, CP Air, the original Frontier Airlines, Midwest Airlines, Northwest Airlines, and locally based Transair operated scheduled flights from Winnipeg to destinations including London–Heathrow, Amsterdam, Glasgow, New York–JFK, San Francisco, Honolulu, Denver, Las Vegas, Chicago–O'Hare, and Minneapolis/St. Paul.

In the early 2000s, CanJet and Jetsgo (both now-defunct) operated nonstop service from Winnipeg to Toronto Pearson International Airport.

On December 10, 2006, the Minister of Transport, Lawrence Cannon, announced Winnipeg International Airport was to be renamed Winnipeg James Armstrong Richardson International Airport in honour of the influential businessman and pioneer of Canadian commercial aviation from Winnipeg. WestJet began seasonal flights to London's Gatwick Airport in May 2016.