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Jon Tenney was raised in Princeton, New Jersey. After graduating from high school, he studied at the Circle in the Square Theatre, acting in over 150 plays, and was accepted into Julliard. Following that he joined the national touring company of Tom Stoppard's The Real Thing, directed by Mike Nichols.

He next played the title role in an off-Broadway production of Tartuffe, which subsequently led to his being cast as the lead in Romeo and Juliet at the Old Globe Theatre in San Diego. A newspaper review of the production came to the attention of the producers of the TV hit Murphy Brown who cast Tenney in the show as Miles' older brother.

Tenney has since appeared on many television series including Crime & Punishment and Equal Justice, co-starring Sarah Jessica Parker. At he same time he starting appearing in films, including Watch It, Fools Rush In and Showtime's original feature, The Twilight Of The Golds, co-starring Jennifer Beals, Faye Dunaway and Brendan Fraser. Among his other credits are roles in Tombstone, Nixon, Music From Another Room, With Friends Like These and in the Sundance hit You Can Count On Me, opposite Laura Linney and Mathew Broderick. Between film work, Tenney has continued to appear on television as a series regular on Steven Bochco's Brooklyn South as well as Get Real and Kristin.

On Broadway he was seen opposite Cherry Jones in The Heiress. Off-Broadway he has starred in The Impossible Marriage with Holly Hunter, Brighton Beach Memoirs, A Shayna Maidel and other productions. In 2004 Tenney starred in the TV pilot Joint Custody and was seen in eight episodes of The Division.