Dublin Airport opened on January 19, 1940, when an Aer Lingus Lockheed 14 departed what was then called Collinstown Airport for Liverpool. It was a modest beginning: one flight a day, grass runways, and a terminal designed to handle just 100,000 passengers a year. That original terminal, designed by architect Desmond FitzGerald, was modeled on the tiered lines of an ocean liner and won the Royal Hibernian Institute of Architects Triennial Gold Medal in 1942. It is today a listed building.

World War II effectively mothballed the airport until 1945. Recovery was swift. By 1947, KLM had inaugurated continental European service to Dublin, and 1958 brought the defining moment in the airport's history: on April 28, Aerlínte Éireann, the predecessor of modern Aer Lingus, operated its inaugural transatlantic service from Dublin and Shannon to New York, making Ireland one of the first nations outside North America with a scheduled transatlantic connection. Passenger numbers topped 1 million by 1963, and Terminal 1 opened in 1972 to absorb the growth.

Today, DUB is the busiest airport on the island of Ireland and recorded over 36.4 million passengers in 2025, its busiest year on record. It is the primary hub for Aer Lingus and the home base for Ryanair, Europe's largest airline. Terminal 2, which opened in November 2010, consolidated all transatlantic operations and houses one of only a handful of U.S. Customs and Border Protection preclearance facilities outside North America, allowing passengers to clear U.S. immigration before departure. A new North Runway opened in August 2022, the airport's first new runway in over three decades, running parallel to and significantly longer than the main existing runway.