In 2000, he moved to Deshler High School in Tuscumbia, Alabama and served as an assistant under AHSAA Hall of Fame coach John Mothershed, until 2004 where he had two undefeated regular seasons.

The following year in 2005, Lindsey became the head coach at Colbert Heights High School Tuscumbia, Alabama for two seasons with a combined record of 14–8.

They represented the West Division in the Conference USA Football Championship Game where they lost to Western Kentucky University.

Lindsey was an offensive analyst on Auburn's staff in 2013, the season the Tigers won the SEC title and fell 13 seconds short of a national championship.

On January 21, 2017, Auburn head coach Gus Malzahn announced that Lindsey would serve as the new offensive coordinator, producing $800,000 in compensation.

[5] He spent one season in Orlando, where they competed for the AAC Championship and the Knights' offense finished 26th nationally in scoring, 11th in yards per game, and 8th in rushing.

Following Phil Longo's departure for Wisconsin, Lindsey was hired by Mack Brown as the Tar Heels' new offensive coordinator and quarterbacks coach on December 15, 2022.

On December 13, 2024, Lindsey was officially hired by Sherrone Moore and the University of Michigan as the offensive coordinator and quarterbacks coach.