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Dillon was born in New Rochelle, New York to second-generation Irish American Catholic parents Paul Dillon (a painter and sales manager for Union Camp, a packing material manufacturer) and Mary Ellen (a homemaker). His brother, Kevin Dillon, is also an actor. Dillon was raised in Larchmont, New York, where he was discovered while attending school. He attended Mamaroneck High School in Mamaroneck, N.Y.

His first role was at age 14 in Over the Edge, which led to roles in Little Darlings (1980) and Tex (1982). In the mid-1980s, Dillon had prominent roles in the Francis Ford Coppola's S.E Hinton adaptions The Outsiders (1983) and Rumble Fish (1983). In 1987, Dillon appeared briefly as a policeman in the music video for the song Fairytale of New York by The Pogues and Kirsty MacColl, a major hit in Ireland and the United Kingdom. In 1989, Dillon won critical acclaim for his performance as Bob in Gus Van Sant's Drugstore Cowboy.

Dillon has had a steady film career after making a successful transition from teenage movies of the 1980s. He continued to work in early 90s with roles in movies like Singles (1992). He had somewhat of a career resurge as the role of Nicole Kidman's husband in To Die For (1995), as well as large roles in Wild Things (1998) and There's Something About Mary (1998), for which he received an MTV Movie Award for Best Villain.

In 2002, he also wrote and directed the film City of Ghosts, starring himself, James Caan and G

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