In a move that could mark the beginning of the end for the Prime Minister, Mr Sunak quit as Chancellor and Mr Javid resigned as health secretary, just minutes after Mr Johnson had issued a humiliating apology for the scandal surrounding former deputy chief whip Chris Pincher.
Four junior ministers followed suit by leaving their roles last night. Nicola Richards, a parliamentary private secretary in the Department of Transport, quit her position in government, while Andrew Murrison resigned as a trade envoy to Morocco and ministerial aides Jonathan Gullis and Saqib Bhatti also quit.
Tory party vice-chair Bim Afolami also sensationally resigned live on TV, declaring of Mr Johnson: “I think it's become clear the time has come for him to stand down."
But Cabinet ministers including Dominic Raab, Liz Truss, Michael Gove, Therese Coffey and Ben Wallace indicated they would be staying in the Government as the Prime Minister appointed chief of staff Steve Barclay as his new health secretary in a hastily-arranged Cabinet reshuffle.
Other ministers were also seen in No 10 last night, including education secretary Nadhim Zahawi.
In his resignation letter, Mr Sunak suggested to the Prime Minister the Government was not being “conducted properly, competently and seriously”.
He wrote: “The public rightly expect government to be conducted properly, competently and seriously. I recognise this may be my last ministerial job, but I believe these standards are worth fighting for and that is why I am resigning.”
Mr Sunak stressed on those occasions where he had previously "disagreed” with Mr Johnson privately, he had support him publicly.
But he added: “In preparation for our proposed joint speech on the economy next week, it has become clear to me that our approaches are fundamentally too different.
“I am sad to be leaving Government but I have reluctantly come to the conclusion that we cannot continue like this.”
Mr Javid told Mr Johnson the British people “rightly expect integrity from their Government”.
In his own resignation letter, Mr Javid wrote: “The tone you set as leader, and the values you represent, reflect on your colleagues, your party and ultimately the country.
“Conservatives at their best are seen as hard-headed decision makers, guided by strong values. We may not have always been popular, but we have been competent in acting in the national interest.
“Sadly, in the current circumstances, the public are concluding that we are now neither.”
He added: "The country needs a strong and principled Conservative party, and the party is bigger than any one individual.
"I served you loyally and as a friend, but we all serve the country first. When made to choose between those loyalties, there can only be one answer.
“It has been an enormous privilege to serve in this role, but I regret that I can no longer continue in good conscience.
“It is clear to me that this situation will not change under your leadership – and you have therefore lost my confidence too”.
Mr Johnson said in letters to both Cabinet members he was sorry to see them resign.
The Prime Minister said Mr Sunak had provided "outstanding service to the country through the most challenging period for our economy in peacetime history", adding: "I have enormously valued your advice and deep commitment to public service and will miss working with you in government".
Former Brexit minister Lord David Frost released a statement saying both Mr Sunak and Mr Javid had done "the right thing” by resigning as he declared the Tory party’s best interests would be served by “new leadership and a new prime minister”.
Former chief whip Mark Harper also posted on Twitter: "Tonight we have seen leadership from Rishi Sunak and Sajid Javid.
"Honourable decisions made by honourable men. The Conservative Party still has so much to offer to our country. It’s time for a fresh start."
Sir Keir Starmer declared the need for “a real change of government and a fresh start for Britain" as he claimed “changing the man at the top won't fix it”.
The Labour leader said in a statement: “After all the sleaze, the scandals and the failure, it’s clear that this Government is now collapsing. Tory cabinet ministers have known all along who this Prime Minister is.
“They have been his cheerleaders throughout this sorry saga. Backing him when he broke the law. Backing him when he lied repeatedly. Backing him when he mocked the sacrifices of the British people.
“In doing so, they have been complicit every step of the way as he has disgraced his office and let down his country. If they had a shred of integrity they would have gone months ago.
“The British public will not be fooled."
Sir Keir ad earlier directly called on ministers to resign. Asked if Mr Johnson was a “pathological liar”, the Labour leader said: “Yes, he’s a liar.
“What we’re seeing this week is a repeat of what we’ve seen so many times, which is Government ministers going out onto the airwaves, giving answers to questions, and no sooner have they finished the media round that the answers they’ve given aren’t accurate because the Prime Minister and Number 10 haven’t been straight with them.
“That is not this week’s story, although it is this week’s story, it’s every week’s story. It’s on repeat, which is why you see the Conservative Party tearing itself apart today.”
First Minister Nicola Sturgeon said “the whole rotten lot” in Mr Johnson’s Westminster government should go.
She posted on social media: “Feels like end might be nigh for Johnson – not a moment too soon.
“Notable tho that the resigning ministers were only prepared to go when they were lied to – they defended him lying to public.
“The whole rotten lot need to go. And needs the permanent alternative of independence.”
SNP Westminster leader Ian Blackford claimed Mr Johnson’s government was collapsing.
He said: "This is the end for Boris Johnson. Tory MPs should have got rid of him months ago – and it speaks volumes they are only acting now out of self-interest and fear they will lose their seats at the next election.”