After a day when the eurosceptic foreign secretary cancelled meetings for crisis talks at his official residence in central London, Johnson chose to walk from his job - just hours after May's Brexit minister David Davis did the same.
"The government now has a song to sing".
Johnson said in his letter that May's plan to keep close economic ties with the bloc means Britain is heading for a "semi Brexit" that would leave Britain with the "status of a colony" of the EU.
Davis said of Mays approach: "It seems to me we are giving too much away too easily".
May appeared in Parliament earlier on Monday afternoon to defend her plan, minutes after Downing Street confirmed the departure of Johnson.
May had been reluctant to spell out her strategy until now precisely for fear of igniting furious rows in her deeply divided Conservative Party.
The plan seeks to keep the United Kingdom and the European Union in a free-trade zone for goods, and commits Britain to maintaining the same rules as the bloc for goods and agricultural products. 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. That timetable looks increasingly optimistic, but European Commission spokesman Margaritis Schinas said the EU was available "available 24/7". Meanwhile, President Donald Trump is scheduled to arrive Thursday for a visit that will be closely watched for any comments on Brexit and US relations with the EU.
Giroud out to show Henry he chose the 'wrong camp'
Hazard said that his country will find it hard to beat France if Chelsea teammate N'Golo Kante "is at his best" for Les Bleus . What's certain is that with one more win Les Bleus are back in the World Cup final for the first time in a dozen years.
In another sign of widespread confusion, Steve Baker, who resigned as David Daviss deputy at the Brexit ministry, charged on Monday that they had been "blindsided" by Mays new proposals.
David Davis said he "wouldn't have done a good job" of delivering May's Brexit plan, with Tory MP Marcus Fysh saying the plan is paramount to breaking manifesto pledges, which "has consequences". "If the Brexit Secretary could not support them they cannot genuinely be delivering Brexit".
International Development Secretary, and one of the most committed Brexiteers in the Tory party, Penny Mordaunt, welcomed the news, but Shadow Brexit Secretary Keir Starmer cast into doubt the efficacy of the new appointee. She did not immediately name a replacement for Johnson. Euroskeptic Conservative lawmaker Peter Bone said party activists felt "betrayed" by the government plan.
May was asked by an opposition lawmaker Monday whether she would contest a vote of confidence if one came rather than resign.
"If she doesn't drop Chequers there will be another", they said, "then another, then another, then another".
"I think it's the wrong thing to do".