Dublin Airport opened on January 19, 1940, when an Aer Lingus Lockheed 14 departed Collinstown (the airport's original name) on a single daily service to Liverpool. The original terminal, designed by architect Desmond FitzGerald, was built to echo the curved lines of a great ocean liner and won the Triennial Gold Medal of the Royal Institute of the Architects of Ireland in 1943; it remains a listed building today. World War II severely curtailed operations, but the postwar years brought rapid expansion.

The airport's transatlantic chapter opened on April 28, 1958, when Aerlínte Éireann (the predecessor of modern Aer Lingus) operated its inaugural Dublin-to-New York service aboard a Lockheed L-1049 Super Constellation, making Ireland the 17th airline to launch scheduled North Atlantic service. A new Terminal 1 followed in 1972, and Terminal 2 opened in November 2010, designed primarily around Aer Lingus operations and transatlantic traffic. Terminal 2 also houses one of only a handful of US border preclearance facilities outside the Americas, allowing passengers to clear US customs and immigration before leaving Irish soil, a practical advantage that has reinforced DUB's role as a preferred transatlantic bridge between Europe and North America.

Situated 7 kilometres north of Dublin city centre, the airport is the primary hub for Aer Lingus and the largest European operating base for Ryanair. In 2025, over 36.4 million passengers moved through its two terminals, a record, placing it among the dozen busiest airports in Europe. A second parallel runway opened in August 2022, adding capacity for the airport's next phase of growth.