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2000s

During the 2000s, representative teams of women's leagues began to enter the FAI Women's Cup. In 2006 a team representing the Galway Ladies League were semi-finalists, losing after extra time and penalties to UCD. A team representing the Mayo Ladies League subsequently defeated UCD in the final. In 2007 the Galway Ladies League reached the final with a team that included Niamh Fahey, Méabh De Búrca and Julie-Ann Russell. All three were also playing for Salthill Devon. On 14 October 2007 at Dalymount Park, Galway defeated a Raheny United team that included Niamh Reid Burke and Olivia O'Toole. Fahey's penalty in the 75th minute gave the Galway Girls a 1–0 win. In 2008 Galway were FAI Women's Cup semi-finalists, losing 2–1 to Peamount United. In 2009 they were beaten 3–2 in the second round by St. Catherine's.

2008–09 UEFA Women's Cup

As a result of winning the 2007 FAI Women's Cup, Galway qualified to represent the Republic of Ireland in the 2008–09 UEFA Women's Cup. They were drawn in Group A9 along with Zürich, Universitet Vitebsk and SFK Sarajevo. The competition format saw Galway travel to Sarajevo in September 2008 to play in a mini-tournament to decide who would progress to the next round. With a squad that included Méabh De Búrca and Julie-Ann Russell, Galway finished second after beating the pre-tournament favourites, Universitet Vitebsk.

Women's National League

In June 2013 the Football Association of Ireland announced Galway as an expansion team for the upcoming 2013–14 Women's National League season. Republic of Ireland women's national football team manager Susan Ronan welcomed the addition of Galway for helping make the league more national. The 2013–14 Galway WNL squad included several veterans of the 2008–09 UEFA Women's Cup campaign including Susie Cunningham, Melissa Casserly and Becky Walsh. Former Galway United manager Don O'Riordan was appointed manager of the women's club in June 2014, replacing Nigel Keady who had overseen the first season.

Galway United

In September 2022 Galway WFC announced that it would "reluctantly" withdraw from the following season's Women's National League: "We hope that other individuals or entities will take up the mantle to continue the tradition of senior and underage women's football in Galway in 2023." The local League of Ireland club Galway United released a statement on 5 October 2022 confirming that they would take over the running of Galway's women's teams for 2023. Phil Trill, who had been Alan Murphy's assistant with Galway WFC in 2022, was appointed as the new head coach. He hoped to secure the bulk of the existing playing squad for the following season.