Dominic Cummings left Downing Street after his relationship with the Prime Minister "fell off a cliff", according to a former Cabinet minister.
Mr Cummings left his role after a power struggle that has rocked the administration, amid claims he had briefed against Boris Johnson and his fiancee Carrie Symonds.
Senior Tory MPs have now called on the Prime Minister to use his departure to "reset the Government" following complaints the party and Parliament were not being listened to during Mr Cummings' time as senior adviser.
It comes after the Daily Telegraph reported Mr Cummings was said to have told colleagues Mr Johnson was "indecisive" and that he and director of communications Lee Cain, who has also announced his resignation, relied on Cabinet Office minister Michael Gove for clarity.
According to the Daily Mail, tensions were raised further when the Prime Minister was shown "hostile texts" briefing against Miss Symonds, which had been forwarded to her.
Prime Minister Boris Johnson with his senior aid Dominic Cummings as they leave Downing Street, central London.
Senior aide to the prime minister Dominic Cummings, in Downing Street in Westminster, London.
Senior aide to the prime minister Dominic Cummings leaves following a cabinet meeting at 10 Downing Street, London.
Dominic Cummings, Chief Advisor to PM Boris Johnson leaves Downing Street for the House of Commons for PMQ's in Central London, UK on October 23, 2019. (Photo by Claire Doherty/Sipa USA
Senior political aide Dominic Cummings speaks to Stuart Wheeler, at his book launch for Winning Against the Odds: My Life in Gambling and Politics, at Carlton House Terrace, London.
Senior aide to the prime minister, Dominic Cummings, at the Conservative Party Conference at the Manchester Convention Centre.
Dominic Cummings arrives in Downing Street, London.
Prime Minister Boris Johnson's former senior adviser Dominic Cummings, sits during the annual Nato heads of government summit at The Grove hotel in Watford, Hertfordshire.
Chief Adviser to Prime Minister Boris Johnson, Dominic Cummings, listens during a press conference at Downing Street, London, on the government's coronavirus action plan.
Dominic Cummings, advisor to the Prime minister arrives in Downing Street with his assistant, Cleo Watson. PA Photo. Picture date: Tuesday April 14, 2020. Prime Minister Boris Johnson remains in Chequers, Buckinghamshire, where he is convalescing following his hospitalisation with coronavirus. See PA story HEALTH Coronavirus. Photo credit should read: Stefan Rousseau/PA Wire
File photo dated 14/02/20 of Dominic Cummings outside his London home, apparently Cummings was spoken to by police after he appeared to have breached government lockdown rules by travelling to Durham when he was supposed to be self isolating in London in late March.
FILE PHOTO dated 26/09/19 of Prime Minister Boris Johnson's senior aide Dominic Cummings. Lockdown questions continue to bombard the Government with the Prime Minister facing pressure to sack his closest aide after it emerged that he travelled to his parents' home despite coronavirus-related restrictions.
Prime Minister Boris Johnson's senior aid Dominic Cummings leaves his north London home, as lockdown questions continue to bombard the Government with the Prime Minister facing pressure to sack his closest aide after it emerged that he travelled to his parents' home despite coronavirus-related restrictions.
Prime Minister Boris Johnson's senior aide Dominic Cummings leaves his north London home, as lockdown questions continue to bombard the Government after it emerged that he travelled to his parents' home despite coronavirus-related restrictions.
A protester outside the north London home of Prime Minister Boris Johnson's senior aide Dominic Cummings , as lockdown questions continue to bombard the Government after it emerged that he travelled to his parents' home despite coronavirus-related restrictions.
Prime Minister Boris Johnson's senior aide Dominic Cummings leaving 10 Downing Street, London, as lockdown questions continue to bombard the Government after it emerged that he travelled to his parents' home despite coronavirus-related restrictions.
Movement in front of Dominic Cummings' house whilst his press conference takes place at Downing Street. *Editors note content*
Dominic Cummings, special advisor for the Government, arriving at his home.
A person walks past a Dominic Cummings protest banner on a roundabout in Wavertree, Liverpool after allegations he breached coronavirus lockdown restrictions.
Dominic Cummings top aide to Prime Minister Boris Johnson arrives at the back of Downing Street after the introduction of measures to bring the country out of lockdown.
A woman wearing a face mask walks past a panel featuring Political advisor Dominic Cummings, UK Prime Minister Boris Johnson and US President Donald Trump.
Caricatures of politicians on large advertisement board for satirical television puppet show Spitting Image inside Westminster Tube Station. (Photo by Keith Mayhew / SOPA Images/Sipa USA)
Senior aide to Prime Minister Boris Johnson, Dominic Cummings, London, ahead of a Cabinet meeting at the Foreign and Commonwealth Office. Picture date: Tuesday September 15, 2020. Photo credit should read: Matt Crossick/Empics
Prime Minister Boris Johnson's top aide Dominic Cummings leaves his home in north London the morning after the announcement that Lee Cain is resigning as Downing Street's director of communications and will leave the post at the end of the year.
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Former Brexit secretary David Davis told BBC Breakfast on Saturday many within No 10 had "turned on" Mr Cummings.
He said: "It is said... people ranging from Allegra (Stratton) – the new spokesman for the Prime Minister – right through to his (Mr Johnson's) fiancee, Carrie, turned against him.
"The relationship with the Prime Minister fell off a cliff. And once that's gone, it's gone."
Mr Davis, who was allegedly described as "thick as mince" and "lazy as a toad" by Mr Cummings when in the Cabinet in 2017, also branded the adviser's style "confrontational" but added the PM had "relied on him" and "there are things he (Mr Cummings) was right about".
There was no sign of Mr Cummings emerging from his north London home on Saturday morning, but his wife Mary Wakefield came outside and told reporters he "would not come out" in the rainy weather.
The BBC reported Mr Cummings' departure had been brought forward given the "upset in the team" and that the PM wanted to "clear the air and move on".
On what could change, Mr Davis told BBC Breakfast: "Well the first thing is there are going to be some new staff in Number 10. He's going to need a new chief of staff who has got to be fiercely efficient but not fiercely political. He's got to find someone who doesn't have their own agenda.
"Secondly, lots of my colleagues in Parliament are hoping for a new relationship with Parliament. More openness, more interaction with Parliament."
Theresa May's ex-chief of staff, Lord Gavin Barwell, also said the departure could lead to more harmonious relations between the Prime Minister and Tory MPs.
Referring to Mr Johnson, Lord Barwell told BBC Radio 4's Today programme: "It feels to me that there's an opportunity here for him to get his Downing Street operation more harmonious and more effective.
"To rebuild relations with Conservative MPs, the parliamentary party.
"And, perhaps, to set a less confrontational and more unifying tone, that is maybe more in tune with his natural instincts."
Some media reports have said Mr Cummings, who left No 10 on Friday carrying a large box, had quit his post with immediate effect.
The PA news agency understands he and Mr Cain will still be employed until the middle of next month, with other reports suggesting Mr Cummings will work from home on projects such as mass testing.
Sir Edward Lister was announced as the interim chief of staff pending a permanent appointment.
The dramatic events have come as Brexit heads to a crucial phase next week, as London seeks a trade deal with Brussels before the end of the transition period on December 31.
The Prime Minister's official spokesman, James Slack, who will replace Mr Cain in the new year, insisted Mr Johnson was not being distracted by the row.
"What the Prime Minister and the Government are focused upon is taking every possible step to get this country through the coronavirus pandemic," he said.