Linehan is the youngest of seven children of william and Margaret Linehan; he has three brothers and three sisters. His Father, Bill (1921–98), was born in Plummer, Idaho, and was the high school principal in Sunnyside, after serving in World War II with the U.S. Army in the Pacific. Both parents and a sister attended the University of Idaho, as did brothers, Ron and Rick, who also played football at Idaho. Ron (1950–2005) was a three-time All-Big Sky linebacker (1969–71) and was selected in the 1972 NFL Draft; he was a high school coach in the Portland area until his death at age 55. Rick had ten career interceptions as a Vandal defensive back (1976–78).

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 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.

The bottom fell out in 2008. After an 0–3 start in which the Rams were outscored 116–29, a significant departure from the days of "The Greatest Show on Turf", Linehan benched Bulger in favor of Trent Green for their game against the Buffalo Bills. The move did not work; the Rams lost 35–14 after allowing 25 unanswered points in the second half. Linehan was fired hours later, tallying an 11–25 record in his 36 games as head coach.

Linehan was announced as the offensive coordinator of the Detroit Lions on January 23, 2009, by new head coach Jim Schwartz. On December 30, 2013, Linehan was relieved of his duties as the Detroit Lions offensive coordinator following the firing of Lions head coach Jim Schwartz.

Linehan inherited a team in transition. Most of the Rams' stars from earlier in the decade had gone elsewhere, and those who were still there had noticeably lost a step. Nonetheless, Linehan's tenure started out on a promising note, as the Rams went 4–2 in their first six games. However, a four-game losing streak in October and November effectively ended any chance of making the playoffs. Despite this slump, the NFC West was so weak that year that while they finished 8–8, missing the division title by a single game. However, the Rams regressed to 3–13 in his second season. Years of questionable draft and free-agent acquisitions caught up with the team, and the season degenerated into a fiasco due to a rash of injuries to the offensive line. The season was also marked by disputes with star players such as Steven Jackson, Torry Holt, and, most notoriously, quarterback Marc Bulger. Holt and Jackson openly feuded with Linehan on the sidelines during games. The easygoing Linehan didn't discipline them, leading to criticism that he wasn't willing to assert his authority.

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.