The Works Progress Administration (WPA) began studying a potential airport for Whatcom County in late 1935 as part of a program to build airports in large Washington cities. A plan to build an airport west of Bellingham was endorsed by the Washington's state WPA office by the end of the year and the head office the following July. On October 20, 1936, Whatcom County purchased 200 acres (0.81 km2) from Charles F. Larrabee to build an airport using WPA funds.

Construction of the airport began on October 22 under the supervision of the WPA. Three runways were planned, but only the first was built initially; it was 3,600 ft (1,100 m) long by 150 ft (46 m) wide, and it was completed and dedicated on June 1, 1940. Temporary Port of Entry status was secured early, but the slow construction left it in a continually tenuous state – United Airlines would only base there if the field were safe enough for their DC-3s, and it maintained its Port of Entry status.

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). The airport opened to the public on December 7, 1941, having employed hundreds of people during its construction. The initial runway, oriented in a northwest-to-southeast direction, was now 5,000 ft (1,500 m) long. The two new runways were another 5,000 ft-long (1,500 m) runway oriented northwest-to-southeast, and a north–south runway that had an initial length of 4,400 ft (1,300 m) but would be extended another 600 ft (180 m) to cross Bakerview Road. 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. During World War II the airport was used by Fourth Air Force for air defense of the Pacific Coast. It was later used by Air Transport Command and Air Technical Service Command as an intermediate ferrying field for Lend-Lease aircraft being flown to Alaska for subsequent transfer to the Soviet Union.

The United States Army Air Forces closed the facility in September 1946, and it was turned over to the War Assets Administration for disposal. A terminal, designed by F. Stanley Piper, was built by United Airlines in anticipation of civilian use. The airport was slowly returned to Whatcom County and redeveloped as a civil airport in the late 1940s. With the rising costs and need for repairs, Whatcom county sold the Airport to the Port of Bellingham for one dollar in 1957. Because of costs, the Port of Bellingham could only resurface the longest of the runways (16/34). Runway 16/34 is still the only runway used as it provides adequate year-round wind coverage for aircraft servicing Bellingham. The airport closed runway 12/30 in 1986, and runway 2/20 was shut down in 1997. The two diagonal runways have fallen into disrepair, their easternmost ends used as taxiways between tarmacs and the sole remaining runway.

Airline service from Bellingham had a modest beginning. 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. By the mid-1980s, Harbor Air had been replaced by San Juan Airlines, a commuter air carrier based in Bellingham which operated shuttle flights to Seattle/Tacoma with Embraer EMB-110 Bandeirante turboprops and Cessna 402 prop aircraft. San Juan Airlines continues to serve the airport at the present time.

In 1985, Pacific Southwest Airlines (PSA) initiated Bellingham's first passenger jet service with McDonnell Douglas MD-80s direct to Los Angeles, San Diego and San Francisco with all PSA flights including a stop at Seattle/Tacoma. PSA was acquired by USAir which continued to serve Bellingham with Boeing 737-300s. Alaska Airlines introduced MD-80 jets in the late 1980s, competing with USAir with both airlines operating nonstop jet service to Seattle/Tacoma and direct one stop service to other destinations. USAir then changed its name to US Airways and eventually merged with American Airlines in 2015; however, by the early 1990s, USAir had ceased serving Bellingham. During the late 1980s, Alaska Airlines was joined by Horizon Air, a wholly owned subsidiary of the Alaska Air Group, with this regional airline flying nonstop service with turboprops to Seattle/Tacoma. 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. Commencing in the late 1980s, United Express was serving the airport with nonstop flights to Seattle–Tacoma International Airport on behalf of United Airlines via code sharing agreements with the respective operating air carriers.