In November 1999 through April 2000, she appeared in Fuddy Meers as Claire at New York City Center, Stage II, for which she received a nomination for the Outer Critics Circle Award as Outstanding Actress in a Play. In March through June 2004, she appeared in the Manhattan Theatre Club Off-Broadway production of Sarah, Sarah. In November through December 2009, she appeared Off-Broadway at the Acorn Theatre in her husband's (Kenneth Lonergan) play The Starry Messenger. From October 2013 to December 2013, she starred in the Off-Broadway Irish Repertory Theater production of Juno and the Paycock as Juno Boyle. The New York Times reviewer wrote: "In one of the finest performances of her distinguished career on the New York stage, Ms. Smith-Cameron imbues her Juno with a steely pragmatism, but more important an emotional pliancy that makes her more prepared than the rest of her clan to beat back the onslaughts of ill fortune that beset them."

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