[4][5] By the end of 1948, most of the property had been acquired, but one of the parcels held out by increasing its selling price each time a purchase offer was made.

New York City Mayor William O'Dwyer suggested that the TBTA get involved, and the authority agreed to build the airline terminal provided that modifications were made to the terminal's design and the airlines agreed to several conditions, including signing binding leases for the term of a bond issue, pledging set revenues, and reimbursing the city for lost revenue on property taxes.

The terminal, which cost $6,841,000 to construct, was built and owned by the TBTA and leased to the East Side Airlines Terminal Corporation, a private entity composed of ten domestic airlines that used the facility: American, Capital, Colonial, Eastern, National, Northeast, Northwest, Pan American, Trans World and United.

[14][15] Upon its opening, the East Side Airline Terminal became the sole point of arrival and departure for all airport buses providing service to and from Manhattan, consolidating bus operations to a single location.

[6][16][17] Buses traveling between the airports and the East Side Airline Terminal via the Queens–Midtown Tunnel brought in additional revenue to the TBTA from the tolls they paid to use the tunnel; previously buses traveling to and from the 42nd Street Airlines Terminal had crossed the East River for free using the Queensboro Bridge.

The rooftop included 275 public parking spaces that were accessed by autos via a separate entrance and ramp at the northwest corner of the building.

At that time, 30 percent of the passengers traveling on the flights from Miami were using buses to the East Side Airline Terminal.

[25] By the early 1970s, most airlines had acquired better ticketing and baggage handling facilities at the airports and more air passengers were traveling to or from the suburbs rather than having trip origins or destinations in Manhattan.

[35] The following year the terminal's rooftop parking was converted to a tennis facility operated by the Murray Hill Racquet Club.

At the time, the Murray Hill Racquet Club was leasing 75 percent of the terminal and subleasing about 185,000 square feet (17,200 m2) to a Werner Erhard est center.