The Mitzi E. Newhouse Theater opened to the public on November 10, 1967. Located in the lower level of the Vivian Beaumont Theater building, this space was originally called the Forum during the residency of the now-defunct Repertory Theater of Lincoln Center.

In 1973, the theater was renamed for Mrs. Newhouse, a prominent New York philanthropist, when Joseph Papp's New York Shakespeare Festival took over the management of the Vivian Beaumont Theater building. The Festival left Lincoln Center in 1978, and in the seven years that followed, the Newhouse was mostly rented to outside producers or was not used at all. A new resident company was formed in 1979, but it only presented two short runs at the Newhouse in 1981.

In 1985, the theater's current management -- Lincoln Center Theater -- was established. Former New York Mayor John V. Lindsay assembled a new board of directors and signed Gregory Mosher as Director and Bernard Gersten as Executive Producer. In 1991, Linda LeRoy Janklow and Andre Bishop succeeded Messrs Lindsay and Mosher as Chairman and Artistic Director. Lincoln Center Theater has not only outlasted all the prior managements combined, but it has become America's largest not-for-profit theater, producing a year-round program of plays and musicals at the Beaumont, the Newhouse and at various other theaters around New York City.