La Plata County Airport opened to commercial airline service in 1946. The first scheduled airline service to the La Plata County Airport began on November 27, 1946, when Monarch Air Lines initiated flights to Denver with stops at Monte Vista, Canon City, Pueblo, and Colorado Springs, Colorado, using Douglas DC-3 aircraft. By April 1, 1947, new routes were added to Albuquerque and Salt Lake City, each making several stops en route. Durango would be the connecting hub for the three routes.

During the summer of 1977, the airport was closed so the terminal building could be expanded and the runway was lengthened to handle jet traffic. Frontier Airlines then began operating Boeing 737 jets to the airport in the fall of 1977. The terminal was greatly expanded again in the 1990s as the airport began seeing a great increase in ski traffic and new service by American Airlines using McDonnell Douglas MD-80 jets. During the 2000s the airport continued to court additional service by new airlines while luring passenger traffic away from the Four Corners Regional Airport serving nearby Farmington, New Mexico.

During the early 2020s, work began on a $28 million terminal expansion project. The project includes, among other things, the construction of two new passenger gates and an expanded passenger hold room, updated security checkpoints, and improved baggage claim facilities. Phase 1A of the project was completed in spring 2024, and work on Phase 1B is expected to be completed by 2026.