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For the first 120 years of its existence, Celtic only fielded male football teams. In the early 1960s, Rose Reilly was noticed by a Celtic scout who wanted to sign her, but the scout found out she was female and withdrew the offer. A women's section was established in June 2007 when Celtic took over Arsenal North L.F.C., founding a Girls and Women's Football Academy at the same time.^{[ – discuss]}

Celtic reached the Scottish Women's Cup final in their inaugural year, losing 3–1 to Hibernian after extra time in May 2008. The team's first silverware arrived two years later as Spartans were beaten 4–1 in the final of the 2010 Scottish Women's Premier League Cup.

In October 2012 Celtic were ejected from the Scottish Women's Cup: they had tried to force the postponement of a quarter final with Glasgow City, but the SWF did not accept Celtic's reason and instead awarded the tie to Glasgow. In August 2013, Celtic faced being thrown out of the national Cup for the second successive season, following a complaint from beaten second round opponents Forfar Farmington: Celtic won the match 5–2, but had named former player Emily Thomson as a substitute in a bid to cup-tie her for the season at her new club, rivals Glasgow City.

At the end of the 2014 season, Celtic saw an exodus of established first team players and promising young prospects, with a number of players making apparent their frustration at the lack of ambition on Celtic's part, as the club had been looking to cut back their involvement in the women's game. Having already lost players of the calibre of Leanne Crichton, Jen Beattie, Christie Murray and Joanne Love, that year the likes of Gemma Fay, Rhonda Jones, Chloe Arthur and Heather Richards also headed for the exit door, while Scotland legends like Julie Fleeting and Suzanne Grant had not committed for the following season (the latter pair did both stay on, but left in 2015).

Celtic reached their second SWPL Cup final in 2017 and their third in May 2018, but were beaten by Hibernian on both occasions; the latter match at Falkirk Stadium finished 9–0, and head coach David Haley said of his beleaguered players: "I'm sure they're as embarrassed as I am". Later that month Haley stood down from first team coaching to concentrate on running the girls' academy. Former Glasgow City coach Eddie Wolecki Black was appointed from Motherwell as his replacement.

Celtic announced in December 2018 that their women's team players would be employed as full-time professionals, with the transition beginning in the 2019 season. In doing so, they became the first ever professional women's football team in Scotland.

Among Wolecki Black's first three signings for the team was his wife, Emma Black. Wolecki Black left his position at the end of the 2019 season, with the club stating in January 2020 they would make further investment to bolster the team's now confirmed status as a fully professional operation.

Fran Alonso was appointed head coach in January 2020, having previously worked under Ronald Koeman at Everton and Mauricio Pochettino at Southampton. In June 2021, Celtic achieved their best showing in the SWPL to date by finishing in runners-up for the third time, but by a margin of only three points to Glasgow City. This saw them qualify for the following season's Champions League for the first time; Celtic were subsequently eliminated from the Champions League at the first qualification round, losing 2–1 to Levante. In December 2021, Celtic won the SWPL Cup by defeating Glasgow City 1–0 in the final, their first trophy since winning the same competition in 2010. Caitlin Hayes scored the winning goal with a header from a Sarah Harkes free-kick, in a match that Celtic dominated and were unlucky not to score more. This was followed by a first ever Scottish Cup victory, beating Glasgow City again, this time 3–2 after extra time.

At the end of the 2022–23 season, Celtic came close to winning their first Scottish title. In a three-way decider on the final day of the SWPL, Celtic had to defeat Hearts while hoping their rivals Rangers could hold Glasgow City to a draw at Ibrox. A Rangers victory would also have been enough for Celtic to clinch the championship, assuming they won their match by a margin larger than Rangers. With Celtic defeating Hearts 2–0 in front of a record attendance of 15,822 at Celtic Park, Glasgow City scored a 92nd-minute winner, taking the trophy away from Parkhead. The following week, Celtic claimed the Women's Scottish Cup for a second time, beating Rangers 2–0 in front of a crowd of 10,446 at Hampden Park thanks to goals from Natasha Flint and Claire O'Riordan.