Despite this morning insisting reports of his exit were wide of the mark, Mr Cummings walked out of Downing Street this evening, perhaps for the last time, brandishing a box that appeared to be the contents of his desk.
It comes during yet another chaotic week that saw the director of communications and a key ally of Mr Cummings, Lee Cain, also stood down.
Mr Cain had been tipped for Prime Minister’s chief of staff job, only for a reported revolt from Tory MPs, ministers and even Mr Johnson’s fiancée Carrie Symonds seeing the former Vote Leave press officer miss out.
Mr Cummings was understood to be furious about Mr Cain’s resignation and had earlier threatened to quit himself during a tense telephone call with Mr Johnson on Wednesday night.
Now after a heated lunchtime discussion with the PM, 231 days since breaching the lockdown rules, Mr Cummings has finally left Downing Street.
A source said: “Their behaviour in the last 72 hours was toxic and Boris said enough is enough.”
Tonight senior Government sources made clear they were not sad to see the back of the controversial Brexiteer.
They said: "In future, advisers will go round the back and let the elected prime minister use the front door."
Another made fun of the foot seen in a picture of Mr Cummings’ exit, which appeared ready to close the door behind him.
They said: “That doesn't happen normally as the armoured door is pulled from the back.
"He's not even out and they are closing it on him. Extraordinary”.
In an extraordinary late-night reshuffle, Mr Johnson has now asked Sir Edward Lister to take on the role of chief of staff for an interim period pending a permanent appointment to the post.
Despite the resignations, Downing Street suggested Mr Cain and Mr Cummings would both still work for the PM and No.10 until mid-December.
Insiders explained this simply was not the case and both men were now on "gardening leave".
A source said: “They absolutely won’t be coming back into the building.”
Tory MPs had earlier welcomed the prospect of Mr Cumming’s exit as an opportunity for a "fresh start".
Senior backbencher Theresa Villiers said: "Clearly there are concerns about the dismissive attitude sometimes shown by Lee Cain and Dominic Cummings towards people in government and MPs on the backbenches.
"And this is an opportunity to move on from that and to have a more collaborative approach."
Sir Bernard Jenkin, chair of the Commons liaison committee, said: "It's an opportunity to reset how the Government operates and to emphasise some values about what we want to project as a Conservative Party in Government.”
Conservative MP Tobias Ellwood suggested it would make things more professional, saying: “Let’s move a little bit away from EastEnders and more to the West Wing.”
The exit also sparked glee among Tory Brexiteers, with influential Tory backbencher Iain Duncan Smith declaring Mr Cummings’ “vision of Government was always doomed to fail”.
He explained: “Rather than some faceless backroom staffer, he is the man who chose to take his family up north during lockdown, appearing to obey a different set of rules than those which constrained the rest of us.
"The good will that the Prime Minister expended on supporting him was deeply damaging.”
Mr Cummings became a household name earlier this year after breaking lockdown rules by visiting his parents’ home in Durham while he was recovering from Covid-19.
The Lancet published a paper by University College London in August looking at the impact of this, finding a “clear decrease in confidence starting on 22 May [when the story of his trip to broke] and continuing to fall quickly in the days following.”
SNP Westminster leader Ian Blackford MP claimed the PM’s “most senior advisers are abandoning the Prime Minister like rats on a sinking ship”.
He said: "If the Prime Minister had a shred of integrity, he would pack his own bags and go with them.
"His tenure has been beset by abysmal failure, utter incompetence, and the alienation of Scotland and the other devolved nations.
Labour MPs also welcomed the announcement, with shadow justice secretary David Lammy saying it was the latest in a series of good news announcements.
He tweeted: “Donald Trump defeated and soon out of the White House. Vaccine breakthrough. Dominic Cummings carrying boxes out of Number 10.
“The crisis we are living through is catastrophic, but my God, it is good to feel hope once again.”
Lib Dem MP Tim Farron shared relief that Mr Cummings was gone, but pointed the finger at Tory MPs for defending him after the lockdown scandal.
He tweeted: “Cummings may have gone, but let's never forget that the worst part of the whole Barnard Castle affair was the way Conservative ministers shamelessly lined up to defend him saying 'it's what any loving father would have done' while millions made huge sacrifices by staying at home.”
The Mayor of Barnard Castle responded by praising Mr Cummings for putting the attraction "on the map" and invited him to apply as a tour guide.
His exit sparked fears from some Brexiteers over what it may mean for Britain’s negotiations with the EU, despite No.10 earlier insisting there would be no change.
Brexit Party leader Nigel Farage tweeted: “It is well documented that I have never liked Dominic Cummings, but he has backed Brexit.
"Seeing him leave Number 10 carrying a cardboard box tells me a Brexit sell-out is close."
Mr Cummings dramatic resignation comes on the same day it emerged the Government settled an employment tribunal claim with a former aide whom he fired.