In his first substantial role, Culkin played the son of a single mother played by Laura Linney in "You Can Count on Me" (2000). Mark Ruffalo co-starred as Linney's troubled younger brother who comes to stay with them when he is down on his luck. The relationship between Culkin and Ruffalo's characters was a major part of the film, and Culkin's careful portrayal of his character was remarkable, especially for a child of only 11 years of age. "You Can Count on Me" was a masterful examination of the human condition, told in the most simple and heartfelt manner. Writer Kenneth Lonergran's directorial debut was lauded almost universally and was awarded the Grand Jury Prize at Sundance later that year.
This auspicious debut soon led to other promising roles for the youngest Culkin. In 2002, he played Mel Gibson's son in M. Night Shyamalan's supernatural thriller "Signs." Next he appeared with Michael Douglas and Bernadette Peters in a dysfunctional family comedy called "It Runs in the Family" (2003). Culkin's short track record already showed a discerning eye for quality films and spoke of nothing less than a bright future for this upcoming young talent, perhaps the most talented of the Culkin clan, and his early talent reached full fruition in writer-director Jacob Aaron Estes' realistic and insightful teen drama "Mean Creek" (2004), in which Culkin played Sam, a young teen terrorized by a seemingly oafish bully, inspiring Sam's older brother and his friends to enact retribution on a boating outing.