Speculation about his future has been growing ever since the shock departure of former chief executive Brian Caldwell before their final home game of the 2022/23 season.
And now a month after the completion of the League One campaign, the club have confirmed Cotterill is no longer the manger of Town.
Cotterill arrived at the Meadow at the end of 2020 having been linked with the club several times before. And at the time he was understood to be a friend of chairman Roland Wycherley.
But after what can only be described as a successful tenure on the pitch – which saw Shrewsbury achieve their second-highest finish in 33 years last season – he has moved on.
His future was first thrown into doubt when the club announced the departure of Caldwell and the creation of a new football board – something the manager had not been consulted on.
Days later, Town approached Cheltenham Town's Micky Moore about becoming their new director of football – something the Shropshire Star understands was in the pipeline long before the approach was made – and again it was something Cotterill had not been made aware of.
The process of forming a new football board without the manager having any prior knowledge suggested plans were being put in place for life after him. And it was at that point fans started to become increasingly concerned about his departure.
The former boss had planned to make decisions about the Town players who were out of contract at the end of the season, but with so much uncertainty around his own future, he had told them he could not give them the answers they needed – and headed back home to Bristol.
Ten days after the end of the season, with Moore now in place, Shrewsbury announced their released and retained list. And now 20 days later Cotterill's time at the club is over.
The first cracks had started to appear in Cotterill's relationship with the hierarchy with comments in the press about his playing budget.
It was early in December when the manager first began to publicly talk about that.
"I think the biggest hurdle for me is going to be finance," when asked about how much business the club would be doing in January.
Town's squad was in fact weakened, numbers-wise in that transfer window, with Aiden O'Brien and Julien Dacosta leaving and only Killian Phillips coming in.
On the pitch, Cotterill squeezed every last drop out of his players – flirting with the play-offs and keeping them in contention for a top-10 position right up until the final day.
However, the budget continued to be a contentious point in post-match and pre-match press conferences as injuries took hold of his squad.
Perhaps the boss felt he was trying to get more money to improve his team, but all that did was strain the relationship further.
Wycherley runs Shrewsbury well and his concern about spending were highlighted when he released a statement just a few days after the completion of the season.
And perhaps the most interesting line in his statement said: "Despite regular financial meetings and warnings that spending is greatly exceeding income and budgets, it continues unabated."
Whatever Cotterill's differences with the club may have been, the hierarchy making big decisions without his knowledge has not done them many favours among fans.
Despite a successful season, it was clear his relationship with the hierarchy had completely broken down.
An emotional Cotterill addressed the press for the final time after the game at Lincoln, saying in public he was not certain about his future – and the fact it took so long to sort out has just increased his support within the fan base.
The Shropshire Star understands there is a 'genuine sadness' among the players and staff that he has gone.
Although he was incredibly demanding, he brought the players through some real adversity last season and they have nothing but respect for him.
So, where does this leave the club?
There is no doubt the pressure is being heaped on Moore and the new management structure at the club.
Peter Brophy is a former police chief inspector, Duncan Montgomery is an accountant and Jamie Edwards' experience in football is limited to the Shrewsbury Foundation.
The decision on Cotterill has taken until now, which means they are already in a race against time to recruit a new manager to prepare for next season.
Players across the country are already in discussions about their futures, so Shrewsbury have some catching up to do.
How they come through the rest of the summer will be absolutely key to how successful they are next season.