The Lucille Lortel Theatre has been in continuous operation as New York's premiere Off-Broadway Playhouse since 1955. In 1999 Lucille Lortel granted the Lucille Lortel Theatre to the Lucille Lortel Theatre Foundation, establishing a new booking policy of non-profit productions only. Since that time it has housed productions such as Arthur Kopit's Y2K (Manhattan Theatre Company), Shakespeare's Cymbeline (Theatre for a New Audience) and Romeo and Juliet (TheaterworksUSA), Lee Blessing's Cobb (The Melting Pot Theatre Company & Trigger Street Productions), and Noel Coward's Suite in Two Keys (Mirage Theatre Company). The Theatre has also been host to numerous benefit performances, readings, and meetings such as: a benefit for the AIDS Theatre Project; an informational meeting regarding 9/11 emergency relief by the New York Foundation for the Arts; and a benefit performance of Watch Your Step, a landmines awareness program sponsored by the Vietnam Veterans of America Foundation.

The Lucille Lortel Theatre was known as the Theatre De Lys until it was renamed in 1981. The Theatre was an anniversary present for Ms. Lortel from her husband, Louis Schweitzer. The landmark production of Brecht/Weill's The Threepenny Opera, starring Lotte Lenya, opened on September 20, 1955, and ran for almost seven years. The production won the Tony® Award for Best Off-Broadway show, helping to put Off-Broadway on the map. The 1950's also saw the inception of the ANTA (American National Theater and Academy) Matinee Series at the Theatre. This series of Tuesday matinee readings began in 1956 and continued for twenty years with the commitment to experiment with unusual dramatic material. The first performance was a verse adaptation of Alan Paton's novel, Cry, the Beloved Country. It was followed by a Shakespearean Variety Show, Lovers, Villains & Fools, with Helen Hayes; Dame Sybil Thorndike, and Sir Lewis Casson in their World Famous Dramatic Recitals; Eugene O'Neill's Before Breakfast with Eileen Heckart; and Langston Hughes' Soul Gone Home and Shakespeare in Harlem with Isabelle Sanford and Godfrey Cambridge.

After The Threepenny Opera closed in 1961, there were a number of successful runs at the Theatre including: Brecht on Brecht with Eli Wallach, Anne Jackson, and Lotte Lenya; Arthur Kopit's Asylum with Anne Francine and George Segal; Sean O'Casey's I Knock at the Doorand Pictures in the Hallway; Sergeant Musgrave's Dance starring Roy Scheider in a cast of 18 with original music by Dudley Moore; Norman Mailer's The Deer Park; Noel Coward's Private Lives with Russel Nype and Elaine Stritch; and Dames at Sea which introduced Bernadette Peters. The ANTA Matinee Series included Ionesco's The Shepherd's Chameleon; An Afternoon of Poetry with Richard Burton and Cathleen Nesbit; Sean O'Casey's Figuro in the Night and The Moon Shines on Kylenamoe; Harding Lemay's Look at Any Man with Billy Dee Williams and Louise Latham; and Athol Fugard's Hello and Goodbye with Kim Hunter and Nicolas Coster.

The excellence established at the Theatre continued with varied productions such as: Kurt Vonnegut's Happy Birthday, Wanda June; Israel Horowitz's Acrobats and Line with Richard Dreyfus and Barnard Hughes, directed by James Hammerstein; Berlin to Broadway with Kurt Weill directed by Donald Saddler; The Web and the Rock directed by Jose Ferrer; Michael Weller's Moonchildren; Tom Cole's Medal of Honor Rag; David Mamet's A Life in the Theatre; and Marsha Norman's Getting Out. The ANTA Matinee Series ended in 1975 after twenty years of groundbreaking performances. The last five years included: A Passage to E. M. Forster with Peggy Wood and Teresa Wright and John Steinbeck's The Long Valley.

The 1980's ushered in Sam Shepard's Pulitzer Prize winning Buried Child; Billy Bishop Goes to War (the first play to move from Broadway to Off-Broadway); Caryl Churchill's Cloud 9 directed by Tommy Tune; Michael Cristofer's The Lady and the Clarinet starring Stockard Channing, directed by Gordon Davidson; Mbongemi Ngema and Percy Mtwa in Woza Albert!, directed by Barney Simon; Wendy Wasserstein's Isn't It Romantic?; Stephan MacDonald's Not About Heroes with Edward Herrmann and Dylan Baker; Gertrude Stein and a Companion with Jan Miner and Marian Seldes; Groucho: A Life in Revue directed by Arthur Marx; and Robert Harling's Steel Magnolias.

In 1990 the Theatre was completely refurbished and was established as one of the most luxurious Off-Broadway Playhouses in New York City. The productions during the decade included: William Finn's Falsettoland directed by James Lapine; Charles Busch's Red Scare on Sunset,starring Charles Busch, Julie Halston, and Mark Hamilton; Jane Anderson's The Baby Dance starring Linda Purl, Stephanie Zimbalist and Richard Lineback; Terrence McNally's Lips Together, Teeth Apart; Larry Kramer's The Destiny of Me with Piper Laurie and John Cameron Mitchell; John Patrick Shanley's Four Dogs and a Bone with Adam Arkin and Polly Draper; and two plays starring Uta Hagen: Nicholas Wright's Mrs. Klein and Donald Margulies' Collected Stories.

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