Dallas Cowboys

Hunter was selected by the Dallas Cowboys in the fifth round of the 2002 NFL Draft.^[2] He was declared inactive for the first 2 games of the season. He also missed 2 games with an ankle injury. He finished the year after playing in 11 games (2 starts), registering 27 tackles (21 solo) and one interception.

The next year, he suffered a fractured left forearm and was forced to miss the first three preseason games. He recovered in time to play in all 16 regular season games and finished with 19 tackles (18 solo), 4 passes defensed and one interception. He played the nickel back role and was one of the leaders in special teams tackles (11).

Hunter entered his third season as the team's starting right corner before suffering an ACL tear in his right knee in the third game of the season and being placed on the injured reserve list,^[3] after registering 9 tackles, one interception, one sack and one pass defensed.

In 2005, it was implied that he might be moved to safety after free agent Anthony Henry was signed to take over the right cornerback job. Hunter and his agent started to ask for a trade and on July 14 he was sent to the New York Jets for a conditional sixth round draft pick in the 2007 NFL Draft (#200-Melila Purcell),^[4] after he stated to the Dallas media that he did not want to be moved to safety and he only wanted to play the cornerback position. In his time with the Cowboys, he racked up 43 tackles and three interceptions in 30 games.

New York Jets

In 2005, the New York Jets acquired Hunter to replace the retired Donnie Abraham at the left cornerback position. Missing some practices early in training camp due to knee swelling, he was waived on August 10, after being on the team for less than three weeks.

Cleveland Browns

On December 6, 2005, the Cleveland Browns signed him as a free agent. He saw action as a special teams player in the last four games but accumulated no statistics. His contract was terminated prior to the start of the regular season on September 2, 2006.

Seattle Seahawks

On January 2, 2007, he was signed as a free agent to the Seattle Seahawks on the recommendation of head coach Mike Holmgren, to provide depth after they lost three of their four active cornerbacks to injury prior to the playoffs.^[5]

On January 6, he played his first game in Seattle, a Wild Card Playoff game against his former team the Dallas Cowboys. Hunter had three tackles, defended one pass, and recovered a Jason Witten fumble. He was also the player who knocked down the Cowboys last second Hail Mary pass to seal the victory. In a postgame interview on the Seahawks team site, he was quoted as saying: "I don't know when I'm going to wake up – I'm not going to go to sleep tonight". This was also the game where Tony Romo serving as the holder for the kicker, fumbled the snap of a potential game-winning field goal with 1:19 to play.

On January 14, he played against the Bears in Chicago in a divisional playoff game. When Rex Grossman underthrew a receiver, Hunter intercepted a pass at a pivotal point in the fourth quarter, preventing the Bears from scoring a touchdown. Unfortunately, the Seahawks threw an interception on the very next play and would lose the game with a field goal in overtime. He was waived on September 1, 2007.

All American Football League

On January 26, 2008, Hunter was selected in the fourth round of the inaugural 2008 AAFL Draft by Team Florida. However, the All American Football League announced that it was postponing its inaugural season until 2009 due to financial constraints.

Dallas Desperados (AFL)

On March 20, 2008, he signed with the Dallas Desperados of the Arena Football League, who were owned by Jerry Jones, who also owned the Dallas Cowboys.^[6] He played in six games with five starts (inactive in five games), registering 23.5 tackles (fifth-most on the team), one interception and three passes defensed. He was placed on the reserve/left squad on June 10, for undisclosed reasons.^[7]

Toronto Argonauts (CFL)

On August 25, 2008, Hunter was signed to the Toronto Argonauts practice roster.^[8] He was released at the end of the training camp on June 25.^[9]