Linney was born in Philadelphia, the son of Maitland (née Thompson) and Romulus Zachariah Linney III. His great-grandfather was Republican congressman Romulus Zachariah Linney.  Linney was raised in Boone, North Carolina and Madison, Tennessee. He earned a Bachelor of Arts degree from Oberlin College and an Master of Fine Arts degree from the Yale School of Drama. He authored three novels, four opera librettos, twenty short stories, and 85 plays which have been staged throughout the United States from South Coast Repertory in California to the Virginia Museum Theater in Richmond, and in Europe and Asia.

His plays include The Sorrows of Frederick, Holy Ghosts, Childe Byron, Heathen Valley, and an adaptation of Ernest L. Gaines’s novel, A Lesson Before Dying, which has been produced in New York and in numerous regional theaters. Many of his plays were set in Appalachia (Tennessee, Holy Ghosts, Sand Mountain, Gint and Heathen Valley), while others focused on historical subjects (The Sorrows of Frederick, King Philip, 2: Goering at Nuremberg). Linney’s vivid biographical reconstructions of controversial personalities are remarkable for their power to retain a lifelike vigor—as in his treatment of Hermann Goering in 2: Goering at Nuremberg, and Lord Byron in Childe Byron.

In 2010 before his death, Linney completed a libretto for an opera based on his first play The Sorrows of Frederick commissioned by The Metropolitan Opera and Lincoln Center Theater. He also completed a full-length play about Alzheimer’s disease, Over Martinis, Driving Somewhere, which received a workshop at New York Stage and Film in the summer of 2010.  Among Linney’s many awards were two Obie awards, one for sustained excellence in play writing; two National Critics Awards; three Drama-Logue Awards; and fellowships from the Guggenheim and Rockefeller foundations, the New York Foundation for the Arts and the National Endowment of the Arts. He was a member of the American Academy of Arts and Letters, which conferred upon him its Award in Literature, Award of Merit and its highest award, the Gold Medal. He received an honorary doctorates from Oberlin in 1994, from Appalachian State University in 1995, and from Wake Forest University in 1998.

He was a member of the Ensemble Studio Theatre, the Fellowship of Southern Writers, National Theatre Conference, College of Fellows of the American Theatre, American Academy of Arts and Sciences, the American Academy of Arts and Letters, and the Corporation of Yaddo. Linney had been chair of the MFA Playwriting program at Columbia University’s School of the Arts and Professor of Playwriting in the Actors Studio MFA Program at The New School in New York. He also taught over the years at Princeton, University of Pennsylvania, Connecticut College, and the Sewanee Writers Conference among others.  Linney was the founding playwright of Signature Theatre Company, which named a theater in his honor in the new Signature Center, which opened in 2012. On his birthday September 21, 2012, the University of North Carolina at its Appalachian State University campus in Boone, NC opened his archives for researchers and scholars.  Romulus Linney died on January 15, 2011, aged 80, from lung cancer at home in Germantown, NY.