Azerrail was founded in 2001 in Baku, Azerbaijan. Under the management of head coach Faig Garayev, Azerrail soon established itself as one of the top clubs in Europe. In 2002, Azerrail won CEV Cup after beating OK Jedinstvo Užice in the final. Azerrail also became the base club for the Azerbaijan national team, producing players such Natalya Mammadova, Valeriya Mammadova, Oksana Kurt, Yelena Parkhomenko and Polina Rahimova.
The team continued to compete in European tournaments in the 2000s and 2010s. In 2011, Azerrail won the CEV Women's Challenge Cup after beating Lokomotiv Baku in the all Azerbaijani final.
After the establishment of Azerbaijan Women's Volleyball League in 2008, Azerrail had a rivalry with Rabita Baku. In the 2015-2016 season, Azerrail won the Superleague title for the first time. As of 2025, Azerrail continues to compete in the league.