Hamilton was first seen nationally on TV, in the movie "The Exchange Student" (CBS, 1985). Small roles, like in "Not My Kid" (also CBS, 1985), and guest spots in the series "Kate and Allie" and "A Man Called Hawk" followed. He appeared as Lovely Mead, one of the turn-of-the-century preppies in PBS's "The Prodigious Hickey" (1987) and its sequels "The Return of Hickey" (1988) and "The Beginning of the Firm" (1989). Hamilton's pensive good looks and sympathetically brainy quality mixed with his low-key style in other specials, such as "Abby, My Love" (a CBS incest drama for which he won a Daytime Emmy in 1991), "Women and Wallace" (PBS, 1990) and Willa Cather's "O Pioneers!" (CBS, 1992).
Hamilton made his film debut in 1984, playing small roles in the dramas "Old Enough" and "Firstborn". He had a tiny role--as Martha Plimpton's boyfriend--in Woody Allen's "Another Woman" (1988). Hamilton stayed away from the big screen until 1993, when he appeared as one of the few surviving rugby players in the true-life plane crash story "Alive" which co-starred Ethan Hawke. He also appeared in Hawke's short film "Straight to One". The weak comedy "With Honors" (1994), as an annoying Harvard undergrad, came next, before he landed his first starring film role. In the twentysomething buddy comedy "Kicking and Screaming" (1995), Hamilton played Grover, a recent college grad whose girlfriend (Olivia d'Abo) leaves him to study in Prague. He next filmed Ismail Merchant's "La Proprietaire" (1996)