Guardiola is the greatest manager in City's history and responsible for building one of the greatest dynasties England football has ever seen - but all good things must come to an end, and his departure signals a new era for the Cityzens.
Enzo Maresca has been appointed in his place and will bring his own ideas to the Etihad Stadium, yet one of the most pressing issues is selecting a new captain in the wake of several experienced players also leaving.
John Stones left the club after 10 years and 295 appearances in Manchester, as did captain Bernardo Silva, who had been at the club for nine years and featured 460 times.
Defensive stalwart Nathan Ake also moved on earlier in the window following 177 matches across a six-year stint.
That degree of experience leaving the club all in one go is nearly impossible to replace - and that's without mentioning the rumoured sale of Ballon d'Or winner Rodri - but Maresca will have to look to those he has inherited for his next club captain.
How do City operate when it comes to captaincy?
While Manchester City do have a traditional captain that wears the armband on the pitch, their method of choosing their leader was slightly unconventional.
Guardiola would allow his players to select who they thought was best for the role - with Silva, Kevin De Bruyne, Kyle Walker, Ilkay Gundogan, Fernandinho and David Silva all taking up the mantle during the Spaniard's tenure (Vincent Kompany held the role before Guardiola joined, and remained captain until departing in 2019).
A leadership group was also selected last summer to help guide the club through the season. Silva, Rodri, Erling Haaland and Ruben Dias were the names chosen by Guardiola.
Of that group, Silva has already left and there is growing noise that Rodri will follow; La Liga giants Barcelona are chasing his signature and reportedly preparing a second bid closer to City's valuation of the midfielder.
That would leave at least two gaps for Marseca to fill before the season begins and a report from The Athletic has stated that he wants to add an English presence to the leadership group, as well as select a captain of his own.
Who is in contention to get the armband?
Haaland and Dias are still at the club and, with both in last season's leadership group, look like decent candidates to take up the captain's mantle.
The latter has been with City since 2020 and has amassed 11 trophies in the last six years while featuring 255 times for the club.
The defender would be a good option to give the armband to and can help guide a new-look Manchester City back into Premier League contention, having been there and done it all before - winning the division four seasons in a row from 2021 to 2024.
It should also be noted that Dias has been named captain in both pre-season matches that he has started so far.
Haaland is likewise a solid choice, with his record-breaking goalscoring helping City to several trophies throughout his stint in Manchester so far.
He is also pretty much guaranteed to play the majority of matches when he's fit, which isn't the same as Dias, who struggled with injury and eventually lost his place in the starting team last season.
There is also, rightly or wrongly, something to be said for the optics of appointing Haaland as captain - the striker is one of the most recognisable footballers on the planet and only grew in stature after a successful World Cup with Norway.
Outside of those two, the reported interest in adding an Englishman to the leadership group is interesting.
Marc Guehi and Phil Foden are the two top English players at the club that also have the experience necessary to be a leader.
The former was captain of Crystal Palace before joining City and has held the armband for the English national team, showing how highly thought of he is behind the scenes.
Foden, meanwhile, is an academy graduate and has been an ever-present in the club's success since breaking into the side, even if his form has dipped in the last two years.
It's a fresh start for everyone under Marseca, though, and the 26-year-old will likely play an important role in the upcoming campaign as he looks to get back to his best.
“Obviously I have been in the club for so long, I am one of the last remaining players to have been here for a long time,” Foden said after signing a new contract.
“So I think I have to be this season, one of the leaders, one of the captains or in and around it for sure.”
Foden took the armband in City's first pre-season fixture this summer.
Outside of the quartet mentioned, it's tricky to see where else Maresca might turn in the search for his new captain.
Gianluigi Donnarumma seems like a solid option, having played top-level football for the best part of a decade, while if you're looking purely at experience, Mateo Kovacic is the most senior player left in the squad.
If there were to be another u-turn in Rodri's future, and he committed his future to the club, he would surely be the best option of those available.
Manchester City are going through a summer of change and Maresca is facing one of his first big decisions as the club's new manager.