Linehan was born and raised in Sunnyside, Washington, about three hours southeast of Seattle, in the lower Yakima Valley of eastern Washington. He was a three-year starter at quarterback at Sunnyside High School, where his father was principal.
Linehan graduated in 1982 and accepted a scholarship to play college football at the University of Idaho in Moscow. He was a member of Dennis Erickson’s first recruiting class as a collegiate head coach. Linehan’s brothers, Ron and Rick, had played at Idaho in the 1970s, and were team leaders on defense.
Linehan was a quarterback for the Vandals under head coaches Erickson (1982–85) and Keith Gilbertson. He redshirted in 1982 and was the back-up to senior All-American Ken Hobart in 1983. Linehan became the starter in 1984 as a redshirt sophomore, but broke his clavicle early in the second game and missed most of that game and two additional starts. The Vandals struggled to a 2–5 record, then won four straight to finish 6–5 and third in the Big Sky. The season concluded with a 37–0 victory in the rivalry game with Boise State in Bronco Stadium.
Linehan led the Vandals to a 5–1 record as a starter in 1985, then a stress fracture in his right foot required surgery and sidelined him for the season. Idaho won the Big Sky title and had consecutive Division I-AA playoff appearances in 1985 and 1986. Finally healthy for a full season as a fifth-year senior in 1986, Idaho went 8–3 in the regular season and he threw for 2,954 yards, ending his college career with over 7,000 yards. Not selected in the 1987 NFL Draft, Linehan signed a rookie free agent contract with the Dallas Cowboys in 1987, but a shoulder injury quickly ended his playing career when he was cut at the start of his rookie training camp.
Linehan began his coaching career as a volunteer coach at Sunset High School in Portland in 1987. At this time he also was helping a friend with his business, selling class rings for Jostens. Linehan’s college coaching career began in 1989 as the wide receivers coach at his alma mater under first-year head coach John L. Smith. After two seasons in Moscow, Linehan coached a year at UNLV, two at Idaho again as coordinator, five at Washington in Seattle under Jim Lambright, and three at Louisville under Smith.
Linehan took his first NFL job as the offensive coordinator/ wide receivers coach with the Minnesota Vikings in 2002. After three seasons in Minneapolis, Linehan served in a similar capacity with the Miami Dolphins in 2005 under Nick Saban, then was hired as head coach by the St. Louis Rams on January 19, 2006. On January 9, 2009, Linehan interviewed with the San Francisco 49ers as a candidate for the open offensive coordinator position.
Linehan was announced as the offensive coordinator of the Detroit Lions on January 23, 2009, by new head coach Jim Schwartz.
On January 27, 2014, the Dallas Cowboys hired Linehan to call plays for the offense, and was later given the title of passing game coordinator. Incumbent offensive coordinator and play caller Bill Callahan remained on staff, but relinquinshed play calling duties and was given the new title of running game coordinator. Linehan serves as the de facto offensive coordinator by leading offensive meetings and calling plays during games. He was formally promoted to offensive coordinator upon Callahan’s departure at the end of the season. Linehan had previously worked with Cowboys head coach Jason Garrett when they served as assistants on the staff of Nick Saban’s Miami Dolphins in 2005.
Linehan and his wife of over 20 years, Kristen, have three sons: Matthew, Michael, and Marcus. He is of Irish descent and is a devout Catholic. Matthew and Michael both currently play college football at the University of Idaho, as their father and uncles did. Matthew is a quarterback and Michael is a linebacker.