[2] Only able to play friendlies in their first season due to the late formation of the club, the team joined the North West Women's Regional Football League the following year.

[10] Although Heath was to die after a brief battle with cancer barely a year after joining the club, Manchester City went unbeaten in the league throughout the 1997–98 season to win the second division title at the first time of asking – their first official silverware.

[14] The step up to the WPL proved to be a large one, however, and the club narrowly avoided relegation on several occasions, never finishing outside of the bottom half for the first seven seasons.

The FA announced that entry would be based on application rather than promotion and that all members of the WPL National Division plus the top two finishers in the two regional leagues would be eligible to apply.

[18] In anticipation of their first WSL season the club began a complete renovation of the playing squad, signing a number of England internationals and promising players, including the likes of England goalkeeper Karen Bardsley,[19] 74-times capped midfielder Jill Scott[20] and new club captain Steph Houghton,[21] intending to make an impression on the league from the start.

Their first season of professional football would see Manchester City finish fifth of eight teams, at the same time winning their first-ever major trophy when they defeated Arsenal in the 2014 FA WSL Cup Final.

Recording twelve wins in their remaining thirteen league games[24] the club entered a title challenge which they only lost on the final day of the season.

Nick Cushing left his role as manager to become assistant coach to Ronny Deila at MLS side New York City, with his last match being against Arsenal on 2 February 2020.

[33] Over the summer of 2022, Manchester City saw nine[35] of its high-profile and established players leave: Bardsley, Scott, and Ellen White through retirement; Janine Beckie to Portland Thorns; Karima Benameur Taieb to Marseille; Lucy Bronze and Keira Walsh to Barcelona; Caroline Weir to Real Madrid; and Georgia Stanway to Bayern Munich.

[34][38][39][33] The last to leave was Walsh, for a world-record transfer fee on 7 September; her departure from Manchester City (after the retirements of Bardsley and Scott) meant that Houghton was the last remaining 2014 season player at the club.

However, the high number of departures at once and the club's seeming lack of sufficient recruitment to cover the calibre of these players were seen as potential matters of concern, with fans decrying the management on social media.

[40] After a rough start to the 2022–23 season,[34] including a first-ever loss to Aston Villa in their first league match,[41] Manchester City re-found their footing and took enough wins to end 2022 fourth in the league, unable to defeat any of the other "Big Four" (the Big Three and newly improved rivals Manchester United) teams but holding strong to retain a position among the title contenders, with the new signings said to have gelled surprisingly quickly.