The attack came at the end of the first day of the Conservative Party's annual conference in Birmingham in which its fault lines over Brexit, already exposed, started to crack open with just weeks to go to settle a withdrawal deal with Brussels. But he has also drawn criticism for his leadership aspirations.
To standing ovations, cheers and laughter, Johnson, May's most powerful critic in her governing party, said her so-called Chequers plan to leave the European Union was a "cheat" that would leave Britain "locked in the tractor beam of Brussels".
"It's always unsafe getting into hypotheticals about what people may or may not say in the future, even if it's just later on today", he said.
While the thrust of his speech was for a change in policy and not a change in leader, the breadth of topics covered and the broad vision Mr Johnson sought to outline will have left those who heard his speech in no doubt that he still has designs on Downing Street.
Johnson said simply that Britain should use a 20-month transition period after Brexit to negotiate a looser, Canada-style free trade deal while stepping up preparations for a "no-deal" exit. But he was quick to add he would stick by May, if not her plan, at least for now. Many took it as mocking May's assertion that the most mischievous thing she had ever done was run through a field of wheat as a child.
"He's too volatile", said Alison Jolley, a party member from just outside Birmingham who cheered loudly for Mr. Johnson during his speech and laughed uproariously at his jokes.
At the foot of the stage there was a press scrum, cameras trained on former Brexit ministers David Davis and Steve Baker in the front row - alongside Stanley Johnson who'd come to see his son.
The comments "brought immediate comparisons on social media to the "lock her up" calls from Donald Trump's supporters about former USA presidential candidate Hilary Clinton", says Business Insider.
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Johnson, the figurehead for the campaign to leave the European Union and the bookmakers' favourite to replace May, has become the loudest critic, warning Conservatives that if they supported Chequers they could be signing up to the party's electoral death.
In fact, Johnson's speech had more than a little of an 80s feel, with the MP aping former-PM Margaret Thatcher calling for a home-owning electorate, while attacking Labour for being anti-aspiration and demanding further tax cuts.
They spend their holidays hiking, and the prime minister enjoys cooking and reading detective novels. May to respond to Mr. Johnson challenge in her speech on Wednesday.
May has had a tough year since a disastrous 2017 conference speech, when she was her plagued by a cough and interrupted by a prankster while parts of the backdrop fell down as she was speaking. "We have that from Theresa May, I think there are others who would struggle to provide that type of leadership", Gauke said.
"This is the moment to chuck Chequers", he said.
But he added: "I believe that when the Prime Minister lands this deal and brings it back, there will actually be a boost to the economy, as businesses start making those investments that they've deferred over the past year or so, consumers start spending on big-ticket items as they feel more confident knowing where we are going in the future".
And she will look to turn the tide of internal party anger towards Jeremy Corbyn's Labour, suggesting on the back of the anti-Semitism row that it is now the new nasty party with the Conservatives as the party of patriotism, business, aspiration and "above all a party of Unionism". And we have a guarantee for the people of Northern Ireland and we are upholding that.