Holcomb was signed by the Tampa Bay Buccaneers as an undrafted free agent after the 1995 NFL draft.
He was also a member of the Indianapolis Colts, Cleveland Browns, Buffalo Bills, Philadelphia Eagles and Minnesota Vikings.
1 ranked Florida State at Doak Campbell Stadium versus a secondary that featured future NFL players Terrell Buckley and Clifton Abraham put him on the map.
He was traded on March 26, 2007, to the Philadelphia Eagles with Takeo Spikes for Darwin Walker and a conditional 2008 draft pick, which the Bills would use to select Stevie Johnson.
On August 27, 2007, the Philadelphia Eagles traded Holcomb to the Minnesota Vikings for a sixth round pick in the 2009 NFL draft.
A Wild Card game against Pittsburgh in January 2003 saw Holcomb, playing for the Browns, become the third quarterback in playoff history to throw for more than 400 yards.
In 2008, Holcomb joined his alma mater Middle Tennessee as the color commentator for the Blue Raider Radio Network.
In February 2015, it was announced that Holcomb would be joining the coaching staff at Riverdale (Tenn.) HS, where he would be handling offensive coordinator duties.