Transport Canada selected the current site for Edmonton International Airport, on the opposite side of the city from the military airport at RCAF Station Namao, and purchased over 28 km2 (7,000 acres) of land. When the airport opened on November 15, 1960, its first terminal was an arch hangar. Today, it is in use by Summit Air. In 1963, a passenger terminal, built in the international style, was opened. It remains in use as the North Terminal. Artwork, fired by Alberta natural gas, adorned the departures area exterior. A large mural, commissioned by the Canadian government in 1963 for $18,000 titled Bush Pilot in Northern Sky by Jack Shadbolt, remains to this day. An appraisal in 2005 indicated that the mural was worth $750,000, and a restoration of the mural was undertaken in 2007.

During the 1970s, the airport experienced rapid growth in traffic as the city of Edmonton grew, and served approximately 2 million passengers by 1980. However, from the early 1980s until 1995, traffic declined. This decline was attributed to the continued usage of Edmonton City Centre Airport as well as to a slowing economy. Edmonton City Centre did not have the facilities to accept large wide-bodied, long-haul aircraft. Thus airlines used City Centre to fly short-haul flights to hubs in other cities where connections to many locations were available.

Growth returned in 1995. In the 1995 Edmonton municipal election, 77% of voters approved by plebiscite to consolidate all scheduled jet passenger service at Edmonton International Airport.

In 1998, the airport began the $282 million "1998–2005 Redevelopment Project". The three-phase project included the construction of the south terminal and central hall concept, a commuter facility, doubling of the apron, and a multistorey parkade. This redevelopment project expanded the passenger capacity to 5.5 million.

By the time the expansion project was completed in 2005, continued passenger growth triggered planning for another expansion. A new 9,900 m2 (107,000 sq ft) control and office tower was added in 2009.

Further expansions completed in 2013 including seven new passenger gates, 14 boarding bridges, moving walkways, and advanced baggage handling and scanning systems. A new Renaissance Hotel was another major addition to the airport landscape.

The airport played a major role during the 2016 Fort McMurray wildfire, operating as hubs for aerial firefighting and medical evacuation. The airport became a way-station and temporary shelter for thousands of Fort McMurray evacuees. The Emergency Operations Centre in the airport ran for 112 hours, organizing the arrival and departure of hundreds of aircraft. During May 2016, the airport saw more than 300 additional daily flights on top of their regularly scheduled service.

In August 2016, the Government of Alberta announced $90 million in funding to begin twinning Highway 19 and that it has protected the area needed for a third runway, which is required due its estimated 3,530 m (11,580 ft) length and orientation as runway 11/29, causing it to exceed current airport boundaries. The airport also plans to extend runway 12/30 by one-third its current length from 3,100 to 4,030 m (10,170 to 13,220 ft) to increase accessibility and capacity tied to Port Alberta Developments/Intercontinental routes.

Historical international airline service

The airport had international service soon after it opened. In 1960, Canadian Pacific Airlines was operating nonstop flights to Amsterdam with Bristol Britannia turboprop aircraft several times a week. By 1961, Canadian Pacific had introduced Douglas DC-8 jetliners on its nonstop service to Amsterdam. Also in 1961, US-based Northwest Airlines was operating daily Douglas DC-7C propliner service on a routing of Edmonton–Winnipeg–Minneapolis/St. Paul–Milwaukee–New York City Idlewild Airport (now JFK Airport). In 1962, Trans-Canada Airlines (TCA, now Air Canada) operated direct flights to London's Heathrow Airport once a week via a stop in Winnipeg and also to Paris Orly Airport three times a week via stops in Toronto and Montreal with DC-8 jets.

During the late 1960s and early 1970s, Pacific Western Airlines operated Boeing 707 charter flights from the airport to the UK and other destinations in Europe. In 1970, Air Canada operated nonstop DC-8 service to London-Heathrow twice a week while CP Air flew nonstop DC-8 service to Amsterdam three times a week. CP Air then introduced Boeing 747 jumbo jet service nonstop to Amsterdam with two flights a week being operated in 1976. By 1978, the airline was also flying nonstop 747 service to Honolulu. Air Canada had also begun daily nonstop Boeing 727-200 service to both Los Angeles and San Francisco by 1979 and was operating direct one stop McDonnell Douglas DC-9-30 service to Chicago O'Hare Airport via Winnipeg by 1985.