Sculptor Alexander Calder was a neighbor; so were choreographer Martha Clarke and members of the experimental dance troupe Pilobolus.

Mentored by professor Arnold S. Eagle, a photographer and cinematographer, Miller began making non-verbal films, which she exhibited along with her artwork.

She played the female lead in NBC's television movie The Murder of Mary Phagan, and supporting roles in feature films, including Regarding Henry (1991), Consenting Adults (1992), and Wind (1992).

In 1991, Miller wrote and directed a short film Florence, starring actress Marcia Gay Harden, about a precociously empathetic woman who acquires the symptoms from others; eventually "catching" a neighbor's amnesia, she forgets her own identity.

For Angela, Miller received the Independent Feature Project's Open Palm Award,[29] and the Sundance Film Festival Filmmaker Trophy from her peers.

"[40] For Personal Velocity, Miller received the Sundance Film Festival Grand Jury Prize and the Independent Spirit John Cassavetes Award in 2002, and the National Board of Review of Motion Pictures Special Recognition for Excellence in Filmmaking in 2003.

Also in 2005, Miller directed her film, The Ballad of Jack and Rose, which stars Daniel Day-Lewis, Camilla Belle and Catherine Keener.

Shot on location in Nova Scotia and on Prince Edward Island, the film is a textured, sorrowful, coming of age story about a 16-year-old named Rose who has grown up in isolation with her father.

[48] A nuanced exploration of a 50-year-old woman's adjustment reaction to moving into a retirement community with her 80-year-old husband, the story flows back and forth between the main character Pippa's memories of her freewheeling New York City youth in the 1970s and her present life.

[49] Miller directed a star-studded cast which includes Robin Wright, Alan Arkin, Keanu Reeves, Winona Ryder and Julianne Moore.

[55][56] In 2013, Miller published Jacob's Folly[57][58] – a complex novel about an 18th-century French rake reincarnated as a housefly in modern-day New York with the ability to enter the other characters’ consciousness and influence them.

[59][60][11][30] Critic Maureen Corrigan praised the work, saying, "Miller's writing style is sensuous, and her individual stories expand, opulently, in scope and emotional impact.

"[61] Miller wrote a screenplay neo-screwball comedy[62] called Maggie's Plan,[63][64] based upon an original story by Karen Rinaldi.

[78] The ensemble cast includes Greta Gerwig, Julianne Moore, Ethan Hawke, Bill Hader and Maya Rudolph.

[83] Miller first met her spouse, actor Daniel Day-Lewis, at a screening of the film adaptation of her father's play The Crucible.