Onstage, she has appeared in The Manhattan Theater Club's "The American Plan", as a repressed young woman romanced by a cad (D W Moffett) and was in the ensemble of Peter Brook's acclaimed production of "The Cherry Orchard" at the Brooklyn Academy of Music and in its subsequent international tour. Miller made her TV debut in the two-part TV-movie, "The Murder of Mary Phagan" (NBC, 1988) and went on to co-star alongside her aunt Joan Copeland in the TNT adaptation of her father's semi-autobiographical play "The American Clock" (1993).

Miller's big-feature credits include Mike Nichols' "Regarding Henry" (1991), in which she played Harrison Ford's mistress, and Alan J. Pakula's "Consenting Adults" (1992), as the ill-fated wife of Kevin Spacey. She also delivered a starling turn as artist Neysa McMein in Alan Rudolph's "Mrs. Parker and the Vicious Circle" (1994).

"I was afraid of the pacivity of the position of the actor," Miller said in 1991. "I'm someone who likes to be in control." Sure enough, she turned to directing and writing, helming "Florence" (1990), a 30-minute film about an amnesiac featuring Marcia Gay Harden. In 1992, Miller directed her first play, a Cincinnati production of her father's controversial "After the Fall", which features a main character based on his one-time wife Marilyn Monroe. Her first feature which she wrote and directed, "Angela", was the story of a little girl who thinks the devil causes her mother's emotional problems. It won the Filmmaker's Trophy at the 1995 Sundance Film Festival.

In November 1996, Miller married actor Daniel Day-Lewis.