He played college football for the Clemson Tigers, and was selected by the San Diego Chargers in the third round of the 2006 NFL draft.

Nicknamed "Clipboard Jesus", Whitehurst also played for the Seattle Seahawks, Tennessee Titans, Indianapolis Colts and Cleveland Browns.

Seattle's front office later stated they had already picked up a potential franchise quarterback in the draft by acquiring Whitehurst with the 2011 selection.

[15] Whitehurst started on January 2, 2011, in a Sunday Night Football game against the division rival St. Louis Rams to determine the NFC West champion.

Prior to the 2011 preseason, Whitehurst was named the backup to Tarvaris Jackson, the former Vikings quarterback whom Seattle acquired in the 2011 offseason.

[17][18] Whitehurst was named the starter for Week 7 against the Cleveland Browns, because Jackson had suffered a pectoral injury against the Giants.

[20] On March 13, 2014, Whitehurst signed a two-year contract with the Tennessee Titans replacing Ryan Fitzpatrick as the backup quarterback.

[26] Whitehurst's best game of the season was on December 27, 2015, against the Miami Dolphins, completing 9-of-14 passes for 78 yards and a 78.9 passer rating.

[30] After starting quarterback Cody Kessler was injured in the first quarter of the Week 5 game against the New England Patriots, Whitehurst completed 14-of-24 passes for 182 yards with a touchdown and an interception as the Browns lost by a score of 33–13.

[31][32] Whitehurst also hyperextended his left knee late in the fourth quarter but returned for the final play of the game, which was a kneel down.