The Airline Terminal Building saw its cornerstone laid by Mayor Fiorello La Guardia on April 22nd, 1940. The building served multiple airline companies, including American, Eastern TWA, United, and PanAm.

This sleek, 5-story Art Deco structure was designed by architect John Peterkin in what was then called the modern-classical style. Its stark, symmetric facade faced Grand Central across 42nd Street. Above the door of the building was a mural depicting a map of the planet, projecting its role as was the gateway to the world.

The terminal provided a convenient Midtown hub for passengers to purchase tickets, have their bags checked, dine, and watch the news in a 600-seat theater before being transported by bus to the airport to catch their flight. The building opened on January 26, 1941, ferrying passengers to the New York Municipal Airport. Soon, it brought passengers to Newark, which opened the same year, as well as Idlewild when it opened seven years later. Inside the terminal, a blue dome raised over gold painted walls, offering an atmosphere that was reminiscent of "Arabian Nights," according to the New York Times.

However, soon after Newark and Idlewild airports opened, buses pulling traffic through grid-locked Midtown stopped seeming like an amenity. A sister terminal opened on First Avenue between 37th and 38th street near the Midtown-Queens tunnel in 1954. The original Airline Terminal Building began to just offer ticketing services.

Declining in value and usage, the terminal was shuttered in 1978 to make way for a corporate headquarters.