Founded in 1964 by George C. White and named in honor of America's only Nobel Prize-winning playwright, The O'Neill is home to six distinct programs: the O'Neill Playwrights Conference, Music Theater Conference, Puppetry Conference, National Theater Institute, Critics Institute and the Monte Cristo Cottage, O'Neill's childhood home located in neighboring New London. At The O'Neill, writers and directors, puppeteers and singers, students and audiences alike take their first steps in exploring, revising and understanding their work and the potential of the theater they help create.

The work of The O'Neill focuses on the script as it begins its journey to the stage. The actors work with minimal props and no sets or costumes, holding scripts in their hands, revealing for the first time the magic of a new play or musical, puppetry piece or cabaret act. Work first performed at The O'Neill has gone on to regional theaters, Broadway, movies and television. Students and professionals who have honed their skills at The O'Neill can be seen in these venues every day across the country. Others work behind the scenes as playwrights, directors, in stage management, publicity and a hundred other roles that the public never sees but are nonetheless essential to every production.

Staff and alumni from The O'Neill have won every major award in theater arts. The O'Neill itself is the winner of a special Tony Award, the National Opera Award, the Jujamcyn Award of Theater Excellence and the Arts and Business Council Encore Award. The seven hundred plays and musicals developed and premiered at The O'Neill include such notable works as August Wilson's Ma Rainey's Black Bottom, Fences, and The Piano Lesson, Nine by Arthur Kopit, Mario Fratti and Maury Yeston, Avenue Q, In The Heights, and Story Of My Life.