For the 1996-97 hockey season, the Columbus Cottonmouths were slated to be one of three new franchises in the Southern Hockey League (SHL). When the SHL folded in the summer of 1996, the Cottonmouths joined the other two expansion entries Macon and Nashville in the Central Hockey League (CHL), creating an Eastern Division along with the Memphis Riverkings, an established CHL franchise, and the Huntsville Channel Cats, the 1996 SHL champion and the only franchise that survived from that league. In its second season, the Cottonmouths won the CHL’s William “Bill” Levins Memorial Cup, defeating the Wichita Thunder in a four-game sweep. The Cottonmouths made the playoffs in each of their five CHL seasons, advancing to the CHL finals in both 2000 and 2001.
In the summer of 2001, the CHL merged with the Western Professional Hockey League. Due to the dramatic changes in travel with the new western cities, only Memphis and Indianapolis remained in the CHL. The Cottonmouths found a new home in the East Coast Hockey League (ECHL). An ownership group consisting of Salvador Diaz-Verson and Shelby Amos purchased the defunct Hampton Roads ECHL franchise, relocating it to Columbus and keeping the Cottonmouths name.
The Columbus Cottonmouths played in the ECHL for three seasons and failed to reach the playoffs each season. Mid-way through their second season in the ECHL, Bruce Garber, the only coach in team history, stepped down. General Manager Phil Roberto took over for the remainder of the season. Prior to the start of the 2003–04 season, Brian Curran took the reins as head coach, with Jerome “Boom Boom” Bechard, the only player to skate with the Snakes in all seven seasons, named Assistant Coach. At the conclusion of the season, Cottonmouths management announced they were moving the franchise to the Bradenton-Sarasota area in Florida. The team, which was later named the Gulf Coast Swords, would never play a single game. Construction began on the new arena but financial problems halted the construction soon after it began. Finally, the ECHL revoked the Swords franchise in the summer of 2006. The partially constructed arena shell stood amid legal battles until it was finally torn down in 2009.
In 2004, the Southern Professional Hockey League (SPHL) was formed following the demise of the South East Hockey League and the World Hockey Association 2. Wanda Amos, the wife of former owner Shelby Amos, obtained a SPHL franchise keeping the Cottonmouths name. Amos hired Columbus hockey legend and coach Jerome Bechard as head coach and general manager. The Snakes won the inaugural SPHL championship in April 2005, going undefeated in postseason play. In 2012, the Cottonmouths won their second President's Cup championship, again going undefeated in the playoffs.
In November 2014, Shannon Szabados became the first female goaltender to win an SPHL game after the Columbus Cottonmouths defeated the Fayetteville FireAntz. Also in that game, Erin Blair and Katie Guay became the first women to referee an SPHL game.
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The Columbus Cottonmouths are currently the longest running professional hockey team in the state of Georgia, having celebrated their twentieth anniversary during the 2015-16 season. Despite their tenure, team owner Wanda Amos announced in March 2017 that she was prepared to suspend operations following the 2017-17 season if new ownership could not be found.
The Cottonmouths went down to the final weekend of the regular season before securing the eighth and final playoff spot. The Snakes finished with a 15-30-7-4 record and faced their in-state rivals the Macon Mayhem in the best-of-three first round. Columbus got some unexpected good fortune when all of the first round games had to be played in Columbus due to a scheduling conflict at the Macon Coliseum. The Snakes took game one by a 1-0 score, and the two teams battled to a scoreless tie through regulation in game 2. But Macon won game 2 in overtime and defeated Columbus in game three.
On May 3, 2017, the SPHL announced that the Columbus Cottonmouths were suspending play for the 2017-18 season. SPHL President Jim Combs stated that "the league is in the final stages of securing new ownership in order to bring the team back for the 2018-2019 season."
In June, New York online real estate broker Fidel Jenkins announced he was finalizing a deal to bring a brand new SPHL franchise to Columbus for the 2018-19 season. Jenkins told the media that the Cottonmouths franchise rights were purchased and re-branded as the Birmingham Bulls, which will begin play in 2017-18. Jenkins also announced that he was given the opportunity to purchase the Cottonmouths name from owner Wanda Amos but declined, saying he wanted to "create something new and turn the page and do something completely different." This effectively ended the longest-running hockey franchise in Georgia history.
However on August 10, 2017, SPHL Commissioner Jim Combs announced “We are no longer considering Fidel Jenkins for membership into the SPHL. It was a decision made this morning by the Board of Governors to terminate his application.”