Barker served as an assistant college football coach at San Francisco State, Occidental, New Mexico State, University of Nevada, Reno, and Pomona-Pitzer. Barker also served as Pomona-Pitzer's head baseball coach concurrent to his work as the Sagehens' offensive coordinator. Barker's CFL coaching career began in 1996 as a member of the Montreal Alouettescoaching staff. The Alouettes set a team record for wins, but lost in the Eastern Division Finals to the Toronto Argonauts. In 1997, he was named the Argonauts' Co-Offensive Coordinator and offensive line coach and was instrumental in guiding one of the best offences in CFL history. In 1999 he replaced the departing Don Matthews as head coach of the Argonauts, becoming the youngest head coach in the CFL. In 2000, he moved back to the United States and was the offensive coordinator of the Los Angeles Xtreme who went on to win the XFL Championship. His work with quarterback Tommy Maddox is well recognized as Maddox went on to win the XFL Player of the Year award and later was named NFL Comeback Player of the Year with the Pittsburgh Steelers. In 2002, Barker was hired to serve as an in-studio analyst on the America One's CFL telecasts, but instead joined old boss Don Matthews as offensive coordinator and quarterback coach of the Montreal Alouettes, leading them to their first Grey Cup in over 20 years. Quarterback Anthony Calvillo enjoyed his finest season as a pro and was the Terry Evanshen Trophy winner as Eastern Division Player of the Year. He moved to Calgary in 2003 where he served as the head coach of the Calgary Stampeders. He was fired after a 5–13 season and was replaced by Matt Dunigan. Barker rejoined the Stampeders in 2005 as general manager. He acquired Henry Burris, Jeremaine Copeland, Rahim Abdullah, and Sandro DeAngelis and played a role in the 2005 CFL Draft, selecting players such as John Comiskey, Brett Ralph, and first overall pick Miguel Robede. These changes helped turn the Stampeders' record from 4–14 to 11–7. In 2006, the Stampeders finished 10–8 and lost to the Saskatchewan Roughriders in the Division Semifinals, 30–21. Barker was replaced as general manager by John Hufnagel after the 2007 season. He was reassigned to the position of Senior Vice-President of Football Operations and director of player personnel. On February 9, 2010, Barker returned to the Toronto Argonauts for his second stint as their head coach. After leading the Argos to the playoffs for the first timesince 2007, Barker assumed the role of general manager on December 15, 2010, replacing Adam Rita, whose contract was not renewed. The CFL announced on February 25, 2011, that Barker was the Coach of the Year for 2010, winning the Annis Stukus Trophy. Prior to the 2012 CFL season, Barker made a trade that brought All-Star quarterback Ricky Ray from the Edmonton Eskimos to Toronto to help an offense that had struggled for some time. That move, and others, helped the Argonauts win the league's 100th Grey Cup at Rogers Centre. After six seasons as the general manager of the Argonauts and compiling a 49–59 record in that time span, Barker was fired on January 24, 2017. Barker spent the 2018 season as a TV analyst on TSN. On January 3, 2019, the Hamilton Tiger-Cats announced Barker would join the team as a football operations consultant. Following the departure of June Jones just prior to 2019 training camp, Barker also added the title of offensive assistant for the 2019 season. For the 2020 season, he was also named a special teams assistant coach.