Miller was born John Anthony Miller in Queens, New York to Mary Claire (née Collins), a teacher, and John A. Miller, an electrician. His ancestry included Irish Catholic “with some admixture of German.” His family moved to Scranton, Pennsylvania in 1941, where Miller was educated at St. Patrick’s High School and the Jesuit-run University of Scranton. He attended The Catholic University of America (CUA) in Washington, D.C. At CUA, he taught drama and English at nearby Archbishop Carroll High School. Miller was launched into stardom in 1973 by winning a Pulitzer Prize for his play, That Championship Season. The original Broadway cast featured Charles Durning, Richard Dysart, and Paul Sorvino. That same year, he was offered the role of the troubled priest, Father Damien Karras, in William Friedkin’s horror film The Exorcist (1973), for which he was nominated for an Academy Award for Best Supporting Actor. After his nomination for The Exorcist, he was offered the lead role in Taxi Driver but turned it down to do Robert Mulligan’s The Nickel Ride.

In 1982 Miller directed the screen version of That Championship Season. Featured in the cast were Robert Mitchum (replacing William Holden, who died before filming began), Paul Sorvino, Martin Sheen, Stacy Keach, and Bruce Dern. His own film career was sporadic, as he preferred to work in regional theater. He starred as Henry Drummond, opposite Malachy McCourt as Matthew Brady, in the Philadelphia production of Inherit The Wind. Miller co-founded the Scranton Public Theatre. With SPT, Miller directed and starred in various productions including Blithe Spirit, Harvey, California Suite, Crimes of the Heart, and The Lion in Winter. He acted occasionally in feature films, including The Devil’s Advocate (1977), The Dain Curse (1978), The Ninth Configuration (1980), Toy Soldiers (1984), The Exorcist III (1990) and Rudy (1993), playing Notre Dame football coach Ara Parseghian. In 1998, he toured the country in his one-man play Barrymore’s Ghost, ending the tour with a four-month run off-Broadway. In October 2000 he performed “Barrymore’s Ghost” in a hugely successful and critically acclaimed production directed by Michael Leland at Theatre Double main stage, in Philadelphia. His last project was a 2001 revival of The Odd Couple for the Pennsylvania Summer Theatre Festival, in which he was to appear in the role of Oscar Madison, but he died before the production opened.

Miller was the father of actors Jason Patric (by first wife Linda Gleason, daughter of Jackie Gleason) and Joshua John Miller (by second wife Susan Bernard). In 1982 Miller returned to Scranton to become artistic director of the Scranton Public Theatre, a new regional theatre company founded the year before. On May 13, 2001, Miller died of a heart attack in Scranton, Pennsylvania, twenty-one days after he had reached the age of 62. In 2004, actor Paul Sorvino, a longtime friend of Miller and a cast member of all three versions of That Championship Season, was commissioned by Scranton to create a bronze bust of the late playwright and actor. The statue was unveiled in December 2008. In March 2011, the first Broadway revival of That Championship Season opened. The cast comprised Brian Cox, Kiefer Sutherland, Jim Gaffigan, and Miller’s elder son, actor Jason Patric. The urn containing Miller’s ashes was placed on the set by his son, who played the role Miller had based on himself.