In 1996, the Columbus Cottonmouths started play in the Central Hockey League, joining the Macon Whoopee and Nashville Nighthawks as expansion entries that were originally slated to be in the Southern Hockey League before its demise in the summer of 1996. Along with the Memphis RiverKings, an established CHL franchise, and the Huntsville Channel Cats, the SHL champion in 1996 and the lone surviving franchise from that league, Columbus and the other two expansion SHL teams formed the new Eastern Division of the CHL in the 1996-97 season. In 1998, the team won the CHL championship, defeating the Wichita Thunder in a four-game sweep. The Cottonmouths were in the CHL playoffs each of their five seasons in the league, making it to the league finals in 2000 before losing to Indianapolis and in 2001 before falling to the Oklahoma City Blazers. In the summer of 2001, the CHL merged with the Western Professional Hockey League and geographic rivalries in Huntsville and Macon were lost, leading the Cottonmouths to seek and obtain entry into the East Coast Hockey League. DVA Sports, composed of owners Salvador Diaz-Verson and Shelby Amos, purchased the defunct Hampton Roads Admirals ECHL franchise, relocating it to Columbus under the Cottonmouths name and logo.
From 2001-2004 the Columbus Cottonmouths played in the ECHL, bringing with them their longtime Captain Jerome "Boom-Boom" Bechard and Head Coach Bruce Garber. In the three seasons that Columbus spent in the ECHL, they failed to make the playoffs. Mid-way through their second season in the ECHL, Garber, the only coach in team history, resigned. General Manager Phil Roberto took over for the remainder of the season. Their best season in the ECHL was their last. Prior to the 2003-04 season the team announced the signing of their new Coach, former NHL tough guy Brian Curran. They finished with a 37-27-8 record, tied with the Greensboro Generals for the best record by a non-playoff team that season. In April 2004, the Cottonmouths management announced their intentions to move their ECHL franchise to the Bradenton-Sarasota area in Florida. The team, which was later named the Gulf Coast Swords, would never come to fruition as financial setbacks delayed the construction of their to-be home arena. Finally, after foreclosure on the arena property and numerous delays, the ECHL revoked the Swords franchise in the league in the summer of 2006.
Southern Professional Hockey League (SPHL): 2004-present
Since 2004 the Columbus Cottonmouths have played as a member of the Southern Professional Hockey League. Led by first year Coach, and Columbus hockey legend Jerome Bechard, the team won the inaugural SPHL championship in April 2005 by first winning a one game playoff against the Fayetteville FireAntz by a 4-2 score. They next swept the regular season champion Knoxville Ice Bears to advance to the league finals, which they won against the Macon Trax with two straight victories, ending with a 3-2 overtime win. The Snakes' victory capped an undefeated postseason in which they won five games without losing a single contest.
In 2006, the Cottonmouths finished with the second-best regular season record in the league but were ousted in the first round of the playoffs two games to one by the Huntsville Havoc.
In 2007 the Columbus team won the SPHL Commissioner's Cup as the team with the best season record, but was ousted in the first round of playoffs by the Jacksonville Barracudas, who won three games to the Cottonmouths' one victory.
In 2008, the Cottonmouths ironically relied on the team that would oust them from the playoffs to get them into the playoffs. On the last day of the regular season, the Knoxville Ice Bears defeated the Huntsville Havoc to give the Snakes the sixth and final playoff berth, which would pit them against first-place Knoxville. The home team won every contest of the best-of-five series with Columbus recovering from an 0-2 deficit with a pair of home wins before losing the deciding contest in Knoxville. The Snakes' 22-24-6 regular-season record was a Columbus hockey team's first losing record since 2002-03 and the first one by a non-ECHL
On April 14, 2012, the Cottonmouths won their second Presidents Cup championship with a two game sweep of Pensacola. The Snakes won Game 1 3-2 at home, Thursday 12 April. They then completed the Championship Seies with a 3-1 road victory over the Ice Flyers. The Cottonmouths went undefeated in the playoffs, 6-0.