Miller attended Yale University and Antioch University, and studied creative writing at the University of California, Los Angeles. In 1997, he published a pseudo-autobiographical novel called The Mao Game about a fifteen-year-old child star attempting to cope with heroin addiction, memories of past sexual abuse, and the impending death of his grandmother, who has been diagnosed with cancer. In 1999, The Mao Game was adapted into a film, written and directed by Miller, and co-produced by Whoopi Goldberg. The film starred Miller, Kirstie Alley, and Piper Laurie, and featured Miller's mother, Susan Bernard, in a brief, uncredited cameo. It toured the festival circuit, and garnered mixed reviews from critics.

Miller began appearing in films and television when he was eight years old. His first film role was in Halloween III: Season of the Witch. He would go on to star in such films as River's Edge, Near Dark, Class of 1999, and Teen Witch. Miller also made guest appearances on several popular television shows, including 21 Jump Street, The Wonder Years, The Greatest American Hero, Highway to Heaven (for which he received a Young Artist Award in 1985), and Growing Pains (hence a popular misconception that he is a relative of Jeremy Miller, who portrayed Ben Seaver on that series; they are not related). Miller appeared in several plays, and was involved in dance from a very early age. He starred in the Los Angeles Ballet Company's production of The Nutcracker for three consecutive seasons beginning at age seven, and later appeared as a Dancer in Janet Jackson's Grammy Award-winning Rhythm Nation 1814 video.

In December 2003, he completed his MFA in creative writing at the University of Iowa. He was awarded the Capote Fellowship, and was also chosen for the Houghton-Mifflin Fellowship Award. He has also written articles for Harper's Bazaar, Playboy, and Esquire. In 2007, Miller appeared as Jinky in The Wizard of Gore. He has written a second novel, titled Ash.

Miller is openly gay and, as of 2013, is in a relationship with fellow Screenwriter M.A. Fortin.

Miller collaborated with M.A. Fortin to write the DreamWorks TV and Fox production Howl. Miller and Fortin then co-wrote the short film Dawn (2014), which was directed by Actress Rose McGowan and premiered at the Sundance Film Festival. The two also co-wrote the screenplay and executive produced the 2015 horror comedy film The Final Girls, directed by Todd Strauss-Schulson and starring Taissa Farmiga and Malin Åkerman. Miller and Fortin wrote the pilot for the USA Network drama series Queen of the South. Miller also serves as an executive Producer for the series, which began airing on June 23, 2016.