Over ninety airlines operate out of JFK. JFK International Airport is the base of operations for JetBlue Airways and is a major international gateway hub for American Airlines and Delta Air Lines. In the past, it has been a former hub for Eastern Air Lines, National Airlines, Pan American World Airways and Trans World Airlines. The airport was renamed after John F. Kennedy, the 35th President of the United States.

The airport is operated by the Port Authority of New York and New Jersey, which also manages the two other major airports in the New York metropolitan area, Newark Liberty and LaGuardia Airport.

JFK Airport was originally known as Idlewild Airport (IATA: IDL, ICAO: KIDL, FAA LID: IDL) after the Idlewild Golf Course that it displaced. The airport was originally envisioned as a reliever for LaGuardia Airport, which had insufficient capacity in the late 1930s. Construction began in 1943; approximately $60 million was initially spent, but only 1,000 acres (400 ha) of land on the site of the Idlewild golf course were earmarked for use.

The project was renamed Major General Alexander E. Anderson Airport in 1943 after a Queens resident who had commanded a Federalized National Guard unit in the southern United States and who had died in late 1942. In March 1948, the New York City Council again changed the name of the airport to New York International Airport, Anderson Field, but the name "Idlewild" remained in common use until 1963.

The Port Authority leased the airport property from the City of New York in 1947 and maintains this lease as of the late 2000s. The first commercial flight at the airport was on July 1, 1948; the opening ceremony was attended by President Harry Truman. Upon opening Idlewild, the Port Authority cancelled foreign airlines' permits to use LaGuardia, effectively forcing them to move to the new airport.

The airport opened with six runways and a seventh under construction; runways 1L and 7L were held in reserve and (as it turned out) never did come into use as runways. Runway 31R (originally 8000 ft) is still in use; runway 31L (originally 9500 ft) opened soon after the rest of the airport and is still in use; runway 1R closed in the 1950s and runway 7R closed around 1966. Runway 4 (originally 8000 ft, now runway 4L) opened June 1949 and runway 4R was added ten years later.

The airport was renamed John F. Kennedy International Airport on December 24, 1963, one month after the assassination of President John F. Kennedy.

The Port Authority originally envisioned a single 55-gate terminal for the airport, but the major airlines of the time did not agree with this plan, arguing that the terminal would be far too small for future traffic. Architect Wallace Harrison then designed a master plan under which each major airline at the airport would be given its own space to develop its own terminal design. This scheme made construction more practical, made terminals more navigable and introduced incentives for airlines to compete with each other for the best design. The revised master plan met airline approval in 1955.

JFK was designed to accommodate aircraft up to 300,000 lb gross weight and had to be significantly modified in the late 1960s to accommodate Boeing 747s.

Airlines began scheduling jets into Idlewild in 1958-59; LaGuardia didn't get jet airliners until 1964, so Idlewild soon became New York's busiest airline airport. During 1960-66 LaGuardia got a new terminal and longer runways, and by the middle 1970s the two airports had roughly equal passenger airline traffic (by flight count, not passenger count). (Until the 1980s Newark was always third place, except during LGA's reconstruction.) The supersonic Concorde, operated by Air France and British Airways, provided scheduled trans-Atlantic supersonic service to JFK from November 22, 1977 until October 24, 2003, when Concorde was retired by both carriers. JFK had the most Concorde operations annually of any airport in the world.[citation needed]