As a player, Frost was coached by Stanford’s Bill Walsh, Nebraska’s Tom Osborne, the New York Jets' Bill Parcells and Bill Belichick, and the Buccaneers' Mike Tomlin and Jon Gruden. In December 2002, while on the Packers' injured reserve list, Frost served as a temporary graduate assistant at his alma mater. He was later a graduate assistant at Kansas State in 2006.
Frost took a position at Northern Iowa in 2007 as linebackers coach before being elevated to co-defensive coordinator one year later. His defense finished the 2008 season tied for third in the FCS in takeaways (40) and ninth in scoring defense (17.7 points per game). The 12–3 Panthers also led the Missouri Valley Football Conference in rushing defense (107.1 yards per game) and scoring defense.
Frost joined Oregon's coaching staff as its wide receivers coach on January 26, 2009. Working under head coach Chip Kelly and offensive coordinator Mark Helfrich, Frost was instrumental in instituting a toughness among his receivers that enhanced their ability as downfield blockers, which contributed to the success of the Ducks’ potent running game. During his four seasons as wide receivers coach, the Ducks reached four straight BCS bowls and three of his departed wide receivers have been invited to NFL camps.
After the departure of Kelly, the University of Oregon promoted Helfrich to head coach and Frost was later officially announced as the offensive coordinator and quarterbacks coach on January 31, 2013.In 2014, Frost was a finalist for the Broyles Award, given annually to the nation's top assistant coach. That season, his protégé Marcus Mariota won the Heisman Trophy en route to a berth in the National Championship game. In his three seasons as the Ducks' offensive coordinator, Oregon recorded a 33–7 record and finished every year among the nation's top six teams in terms of both scoring offense and total offense.
On December 1, 2015, Frost was hired as the head football coach at the University of Central Florida. Frost replaced long time UCF head coach George O'Leary and interim head coach Danny Barrett, who took over the Knights when O'Leary resigned following an 0–8 start. The Knights went on to finish 0–12 that year. Frost immediately turned UCF around. He won six games in 2016, taking the Knights to the 2016 Cure Bowl, where they lost to Arkansas State. In 2017, the Knights stormed through the regular season, finishing 12–0. They won The American championship game at home against Memphis.
On December 2, 2017, Frost accepted the head football coach position at the University of Nebraska–Lincoln. Despite this, Frost led the Knights into the 2018 Peach Bowl–the school's second-ever appearance in a major bowl. In that game, they defeated 7th ranked Auburn, completing the first undefeated and untied season in school history. Following the game, the school claimed a national championship.