Dulles has been the backdrop for many Washington based movies, starting shortly after the airport opened with the 1964 film Seven Days in May.

The 1983 comedy film D.C. Cab,starring Mr. T, Adam Baldwin and Gary Busey showed scenes outside of the main terminal at Dulles Airport.

The action movie Die Hard 2: Die Harder is set primarily at Dulles airport. The plot of the film involves the takeover of the airport's tower and communication systems by terrorists, led by Colonel Stuart (William Sadler), who subsequently uses the equipment to prevent airliners from landing, demonstrating the consequences by fooling one jet into crashing onto a runway. It is up to former NYPD cop John McClane (Bruce Willis) who is currently with the LAPD, to stop them from downing more planes, one of which has his wife aboard. The film was not shot at Dulles; the stand-ins were Los Angeles International Airport (LAX) and the now-closed Stapleton International Airport in Denver. An often-noted inconsistency is the existence of Pacific Bell pay phones in the main terminal (the telephone company that served Dulles at the time was GTE and the nearest PacBell territory was thousands of miles away).

Portions of all three sequels to the disaster film Airport were filmed at Dulles: Airport 1975, with Charlton Heston, Karen Black and George Kennedy; Airport '77, with Jack Lemmon, Christopher Lee and George Kennedy; and The Concorde: Airport '79.

Dulles has also served as a stand-in for a New York City airport, in the 1999 comedy, Forces of Nature. While set in a New York airport, the main terminal is recognizable.