[8][9] On October 20, 1936, Whatcom County purchased 200 acres (0.81 km2) from Charles F. Larrabee to build an airport using WPA funds.

[citation needed] In 1940, the United States Army Corps of Engineers took over the project and expanded the airport to three full runways, revetments for parking aircraft, and development of personnel quarters on 350 acres (140 ha).

[citation needed] The airport opened to the public on December 7, 1941, having employed hundreds of people during its construction.

[13] Following the Attack on Pearl Harbor the same day, Whatcom County offered the use of the airport to the U.S. military, who seized it on December 10.

The United States Army Air Forces closed the facility in September 1946, and it was turned over to the War Assets Administration for disposal.

With the rising costs and need for repairs, Whatcom county sold the Airport to the Port of Bellingham for one dollar in 1957.

During the late 1970s and early 1980s, Harbor Airlines, a commuter air carrier based in Washington, operated nonstop shuttle service to Seattle–Tacoma International Airport with small Britten-Norman Islander twin prop aircraft.

[19] Aircraft operated by Horizon Air into the airport over the years included such propjets as the Fairchild Swearingen Metroliner, the de Havilland Canada DHC-8 Dash 8 and the Dornier 328.

Horizon Air, which currently operates flights for Alaska Airlines, continues to serve Bellingham at the present time with nonstop service to Seattle/Tacoma flown with the Embraer E175.

There was one concession stand: Halibut Henry's store, where light snacks, coffee drinks, gifts, and sundries were offered.

The early 21st century saw rapid expansion at the Bellingham International Airport from several air carriers operating mainline jet aircraft with these airlines being motivated by the potential passenger loads from lower mainland British Columbia in Canada.

Between June 2006 and April 2008, Delta Air Lines also used to serve Bellingham with flights to Salt Lake City operated by their regional affiliate SkyWest Airlines.

In 2012 Allegiant announced service to two locations in the Hawaiian islands (Honolulu and Kahului) from Bellingham after receiving ETOPS certification from the FAA for their 757 aircraft.

Allegiant has also unsuccessfully tried serving other markets from Bellingham in recent years, such as Denver, Tucson, Reno, and Anchorage.

[25] This project was completed in order to serve Allegiant 757 service to Honolulu and Maui which began operations in November 2012.

In early 2012, Frontier Airlines announced the addition of a daily seasonal summer service from Bellingham to its main hub in Denver beginning May 2012.

[23] The Washington Air National Guard (WANG) once occupied a 7.5-acre site at Bellingham International Airport.

This merged airline offers scheduled and charter flights from Bellingham to the San Juan Islands in Washington, Seattle, Tacoma, Port Angeles, Olympia, and British Columbia.

[23] Northwest Sky Ferry and San Juan airlines offer prop aircraft service with Cessna 206, 207 and 182 airplanes.

[29] On April 25, 2024 Southwest Airlines announced it will halt operations at Bellingham International Airport (Denver, Las Vegas, Oakland) after August 4, 2024.