Indianapolis International Airport (IND) opened on September 24, 1931, formally dedicated as Indianapolis Municipal Airport after airline traffic first operated from the field in February of that year. It replaced Stout Field as the city's primary commercial aviation facility. In 1944, the airport was renamed Weir Cook Municipal Airport to honor Colonel Harvey Weir Cook, a World War I flying ace from Indiana. The name Indianapolis International Airport followed in 1976, coinciding with the opening of a new international arrivals facility.

The airport's jet age began on April 30, 1961, when Trans World Airlines inaugurated nonstop service to New York City using a Convair 880. That connection to TWA ran deep: the airline's predecessor, Transcontinental Air Transport, had made Indianapolis a stop on the first transcontinental air and rail service between Los Angeles and New York as far back as 1929. IND's cargo identity is equally defining. The FedEx Express hub opened at the airport in October 1988 and has grown into the world's second-largest FedEx facility, trailing only the carrier's SuperHub in Memphis.

The current terminal, the Colonel H. Weir Cook Terminal designed by HOK architects, opened in 2008 as the first post-9/11 greenfield airport terminal built in the United States and the first complete airport campus in the country to earn LEED certification. Positioned midfield between the 2 parallel main runways, the 40-gate terminal is organized around a central civic hall beneath a 200-foot diameter skylight. The airport sits roughly 7 miles southwest of downtown Indianapolis, generating an estimated $7.5 billion in annual economic impact for Indiana.