May's proposals for a future European Union relationship after Britain departs from the bloc next March had taken two years of internal government wrangling to agree, but within 48 hours Johnson and Davis had resigned saying they could not back the plans.
But it soon began to unravel when Davis resigned late on Sunday and launched a no-holds-barred attack on her plan, calling it "dangerous" and one which would give "too much away, too easily" to European Union negotiators, who would simply ask for more.
Johnson's departure came a day after David Davis, the British minister in charge of Brexit negotiations, also stepped down in protest of May's new Brexit strategy that pointed to a more "business-friendly" deal with the EU.
The ex Foreign Secretary said Mrs May was putting Britain on a track to having "the status of a colony".
Mr Davis, who has been Brexit Secretary since Mrs May became prime minister in 2016, said he had made compromises since taking on the role, but this was "one compromise too far". "The trouble is that I have practiced the words over the weekend and find that they stick in the throat".
May met with Conservative lawmakers in a packed room at Parliament, in a bid to calm the feverish atmosphere in the deeply divided party. As we developed our policy on Brexit, I have allowed Cabinet colleagues considerable latitude to express their individual views.
Earlier, May defended her Brexit plan to lawmakers in the House of Commons, with Johnson absent from his usual place on the Conservative front bench.
Under her proposal, a treaty would be signed committing the UK to "continued harmonisation" with EU rules - avoiding friction at the UK-EU border, including Northern Ireland.
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She added: 'If you are not able to provide the support we need to secure this deal in the interests of the United Kingdom, it is right that you should step down'.
Government unity began to fray within hours.
Johnson's replacement has not yet been announced, while May replaced Davis with Dominic Raab, the former housing secretary and also a pro-Brexit advocate. In his resignation letter to May, Davis said the policy "hands control of large swathes of our economy to the European Union and is certainly not returning control of our laws in any real sense".
Johnson reportedly was more blunt, describing the plan as a "turd". At the time, there were calls for her resignation - and now, she's facing even more pressure. "The Prime Minister can't deliver Brexit and has zero authority left".
Some Conservative Party lawmakers warned they would not tolerate a betrayal of Brexit.
May was asked by an opposition lawmaker Monday whether she would contest a vote of confidence if one came rather than resign. We had wanted to lower the cabin windows to improve visibility; and even though such designs were already on the market, and even though there had been a horriﬁc spate of deaths, mainly of female cyclists, we were told that we had to wait for the European Union to legislate on the matter.
The man leading the UK's negotiating team, David Davis, resigned late on Sunday night, saying that he did not agree with the UK's proposals, so was the wrong person to be going into negotiations with them.