Informed sources on Monday night suggested Cockerill had been ousted after what amounted to a player coup, with senior members of the squad informing the board that it was high time for a change.
There was disharmony between Cockerill and his head coach Aaron Mauger, two very different characters who had apparently long since realised they did not see eye-to-eye.
It is understood that Mauger, an ex-All Black and former Leicester centre, made it known that he was unable to work with Cockerill. One source claimed that after defeat against Wasps at Welford Road in September, Cockerill was in the midst of a post-match rant in the dressing room when Mauger, who favours a more softly-softly approach, asked him to leave.
Among the players, there had been a growing realisation that the status quo could not survive. It is thought that there are many members of the Leicester squad who have been aligned with Cockerill and others more inclined to side with Mauger in what became a clash of cultures.
Just last week, following Bristol's decision to oust their director of rugby Andy Robinson, Cockerill spoke about the need for rugby to avoid going down the same hiring-and-firing path as football. Yet, within days, he was removed from a prestigious post he had held since April 2009.
Any sense that Mauger, who came to the club with a glowing reputation, will simply pick up the baton is apparently wide of the mark. The New Zealander will take over on an interim basis but he may also be on his way out at the end of the season unless there is a remarkable about-turn.
Instead, the initial intention is thought to involve building a new coaching regime around another club stalwart, former Ireland full back Geordan Murphy.
For now, there is also likely to be a potentially damaging recruitment hiatus as prospective signings await clarification about the direction the Tigers are taking.
Cockerill will be a hard act to follow. He was a fervently committed leader and Leicester man to his boots who achieved success over a sustained period.
In his official statement, he said: 'It is with great sadness and regret that I leave my position. I still believe that I am the right person to lead the team. I arrived back at the club in 2004 as an academy coach and leave as director of rugby with a record that stands up against any in club rugby in the world.'
Leicester's England scrum-half Ben Youngs paid tribute to the departing coach on Twitter, saying: 'He gave me my shot and I enjoyed success under him. His commitment and passion for Leicester Tigers was everything that the club's about.'
It won't be long before speculation is in full swing, with Stuart Lancaster doubtless among those who will be linked with the Leicester job. Cockerill could swiftly resurface at Worcester, who are seeking a hard-hitting director of rugby.
Meanwhile, Leicester and England centre Manu Tuilagi is understood to have had a scan on Monday amid fears that he has suffered a medial ligament injury to his right knee after being helped off in the seventh minute of his side's loss to Saracens on Sunday.
The RFU also revealed that Chris Robshaw has been sent for a scan on his injured shoulder.