In a day filled with drama, the PM finally caved to party pressure after admitting he failed to persuade his remaining cabinet colleagues he could fight on following a record-breaking mass exodus of his top team.
‘In politics, no one is remotely indispensable,’ a frustrated Mr Johnson acknowledged in a statement delivered from a lectern in Downing Street.
‘I want you to know how sad I am to be giving up the best job in the world, but them’s the breaks,’ he added.
A new Tory leader will now be elected who will replace Mr Johnson in No 10.
But the PM shrugged off calls for him to leave Downing Street immediately, confirming instead he would remain in post until a new premier is elected.
The move enraged his critics and ignited a fresh wave of resistance in the Tory party following an embarrassing week of chaos in Westminster.
Former Conservative prime minister Sir John Major intervened in the wake of Mr Johnson’s speech, warning it would be ‘unwise’ for him to remain in office while a new Tory leader is elected.
He instead called for deputy prime minister Dominic Raab to serve as acting prime minister until a new leader is elected.
In a letter to Tory 1922 Committee chairman Sir Graham Brady, Sir John added: ‘The proposal for the prime minister to remain in office – for up to three months – having lost the support of his cabinet, his government and his parliamentary party is unwise, and may be unsustainable.
‘In such a circumstance the prime minister maintains the power of patronage and, of even greater concern, the power to make decisions which will affect the lives of those within all four nations of the United Kingdom and further afield.
‘Some will argue that his new cabinet will restrain him. I merely note that his previous cabinet did not – or could not – do so.’
The concerns were echoed by Stephen Morgan, Labour MP for Portsmouth South, who said: ‘The prime minister's tone-deaf statement to the country is another reminder that he is incapable of leading. He must go and go now.
‘He cannot be allowed to cling on for months and further distort the important business of government toward his own ego.
‘If he doesn't, the Labour Party will take responsibility and bring a vote of no confidence in the national interest.’
Mr Johnson has already appointed new cabinet ministers to replace the dozens who quit as part of a mass revolt, protesting his leadership.
In a statement in Downing Street, the PM conceded: ‘It is clearly now the will of the parliamentary Conservative Party that there should be a new leader of that party and therefore a new prime minister.
‘And I’ve agreed with Sir Graham Brady, the chairman of our backbench MPs, that the process of choosing that new leader should begin now and the timetable will be announced next week.
‘And I’ve today appointed a cabinet to serve, as I will, until a new leader is in place.’
But in an unapologetic resignation statement, Mr Johnson said he had fought to stay on because of a sense of ‘duty’ to the ‘millions of people who voted for us’ in 2019 when he won a landslide election victory.
‘I have tried to persuade my colleagues that it would be eccentric to change governments when we are delivering so much and when we have such a vast mandate and when we are actually only a handful of points behind in the polls,’ he said, as crowds jeered ‘bye bye Boris’.
But ‘I regret not to have been successful in those arguments and of course it is painful not to be able to see through so many ideas and projects myself’.
Since Tuesday evening almost 60 MPs have quit government or party posts and on Thursday morning newly-appointed chancellor Nadhim Zahawi went public with a call for Mr Johnson to go.
‘As we’ve seen, at Westminster the herd instinct is powerful, when the herd moves, it moves,’ the prime minister said.
It is hoped a new Tory leader could be in place at No 10 by the next Conservative party conference in October.
However, Gosport MP Dame Caroline Dinenage has warned this is not good enough.
The former health minister believed the PM was ‘not governing’ in the ‘best interests’ of the country.
‘We need to accelerate this leadership process as quickly as possible and get a new team in place – we owe it to the country,’ she said.
‘We need a fully-functioning and operational government in place, we need people with leadership, integrity, vision and we need them in place quickly.’
Tory leadership hopefuls are now preparing for a potentially bitter contest over the summer.
Fareham MP and attorney general Suella Braverman has already thrown her hat in the ring to become the next prime minister, announcing the move on Wednesday evening during ITV’s Peston talk show.
Arch-Brexiteer Steve Baker has also indicated he will run.
Meanwhile, Portsmouth North MP Penny Mordaunt – who the bookies have tipped as a front-runner in the leadership contest – is yet to make any formal statement about any ambitions to lead the Tories.
Under the expected timetable, Conservative MPs will take part in a series of votes to whittle leadership candidates down to two, with Tory members then deciding the winner.