Seven of the 30 ministers present at the meeting spoke out against May's Brexit plan but all MPs backed it by the end of the summit.
Chief whip Julian Smith was inviting MPs to Downing Street to hear from the Prime Minister's chief of staff Gavin Barwell for a briefing on the Chequers proposals in a bid to win them round ahead of Monday's meeting.
Despite his reservations, Mr Johnson fell into line along with the rest of the Cabinet's Brexit-backing ministers. He said the same sentiment extended to Johnson as well. Meanwhile, President Donald Trump is scheduled to arrive Thursday for a visit that will be closely watched for any comments on Brexit and USA relations with the EU.
One other element of Friday's agreement worth noting is that it pledged to speed up preparations for the United Kingdom to be ready to leave the European Union without a Brexit deal in March next year.
"I'm afraid this is nonsensical fudge from the UK Government", said David Henig, a former UK trade negotiator and director of the European Centre for International Political Economy.
May's office confirmed that Davis had resigned but had no comment yet on the reasons.
Critics of Brexit found such admissions astounding and evidence of chaos and lack of leadership - two years after the referendum and eight months before Britain leaves the union.
Asked if it was everything he hoped for, Mr Gove told BBC's Andrew Marr Show: "No, but then I'm a realist and one of the things about politics is you mustn't, you shouldn't make the ideal the enemy of the good".
Other EU leaders have cautiously welcomed May's proposal.
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Environment Secretary Michael Gove said Sunday that it did not contain everything he wanted but "I'm a realist".
"That is not something that this country voted for, it is not what the prime minister promised", he told BBC radio. "In practice, it is not doing so". But talks in Brussels were notoriously slow, mostly because Mays government could not - and still cannot - agree on what kind of future relationship Britain wants with Europe on trade, immigration, law, tariffs and border checks and security. It was a rare consensus, following talks at her Chequers country retreat about the way forward - a move meant to kick-start talks with the European Union that have been stalled for months.
"Grassroots party members will have no truck with their perceived treachery. No one in the world is as much to blame for this monumental mess as himself".
UK Prime Minister Theresa May is trying to finalize a detailed proposal to put to the European Union in the final stages of the negotiations, but has been thwarted by a cabinet riven by different visions of what Brexit should, or can, accomplish.
Cabinet Brexiteers have already been persuaded to support the plans after the marathon session of talks at Chequers on Friday, but backbench Eurosceptics have expressed grave doubts.
Her strategy pushes to keep Britain inside a free-trade area for goods with the EU, while also committing to ending the free movement of people and the supremacy of the European court.
Just 48 letters from MPs are needed to trigger a vote of no confidence in Mrs May, but it is understood the PM's team is increasingly confident that she will be able to see off any bid to topple her. Some Brexit backers cheered Davis on. Well done David Davis for having the principal and guts to resign. "This maintains high standards in these areas, but we will also ensure that no new changes in the future take place without the approval of our parliament", she explained.
Jeremy Corbyn, the leader of the opposition Labour Party, tweeted that the resignation "at such a crucial time" showed that May "has no authority left and is incapable of delivering Brexit".
"Those of us who believe that we want to execute a proper Brexit, and one that is the best deal for Britain, have an opportunity now to get behind the prime minister in order to negotiate that deal", he said.