May hammered out a compromise with her deeply divided cabinet in an all-day meeting on Friday, but after consulting friends and allies since, Johnson decided he could not promote the deal.
A Downing Street spokesman said: “This afternoon, the prime minister accepted the resignation of Boris Johnson as foreign secretary. His replacement will be announced shortly. The prime minister thanks Boris for his work.”
After the Friday meeting, it emerged that Johnson had referred to attempts to sell the prime minister’s Brexit plan as “polishing a turd”.
His resignation follows that of the Brexit Secretary David Davis, and his No 2 at the Department for Exiting the EU, Steve Baker.
As the flamboyant public face of the 2016 campaign that persuaded Britons to quit the European Union, known commonly as Brexit, Johnson’s departure will deepen the sense of crisis around May, and increase the chances that she could face a vote of no confidence.
Johnson is perhaps the most high-profile advocate of Brexit and his departure underscores the depth of the divisions within May’s bitterly divided government
If 48 MPs write letters of no confidence, May will face a vote of no confidence. Many of the prime minister’s supporters believe she would win such a contest, but if she lost, May would face a leadership challenge, with Johnson among the potential candidates.
In Davis’s resignation letter, he said he believes May’s proposal for a UK-EU free trade area governed by a “common rule book”, “hands control of large swathes of our economy to the EU and is certainly not returning control of our laws in any real sense”.
Davis was among the members of the prime minister’s cabinet demanding a more complete break from the European Union, known as a “hard Brexit”
May moved swiftly on Monday to try to stabilize her government by appointing Dominic Raab, another advocate of Brexit, to replace Davis, although Johnson’s decision will reverberate.
Davis said that he could not accept the approach that May demanded in the meeting with top officials on Friday, contending that Britain was giving away too much, too easily in negotiations with the union, and that he was leaving his job because he could not, in conscience, argue for the cabinet’s Brexit position in public.
Other members of May’s cabinet have been arguing for a “soft Brexit,” which would seek to maintain economic stability by keeping closer ties to the European Union after Britain leaves.
Britain faces a deadline of March 29, 2019, to reach a deal with the EU. Progress has been slow and difficult, but May appeared to have taken a big step on Friday in the meeting with her cabinet by bringing advocates of a hard-line Brexit into line.
The Guardian and The New York Times contributed to this story.