The former Foreign Secretary crashed through the first day of the Tory conference in Birmingham, saying the Chequers plan was “entirely preposterous” and suggesting that Theresa May wasn’t committed to delivering Brexit.
It brought a sharp response from Brexiteers and Remainers, with the former Brexit Secretary David Davis mocking Mr Johnson’s plans for a bridge linking Britain and Ireland, and Scottish Tory leader Ruth Davidson calling for a “period of silence”.
Mrs May insisted she was acting in "the national interest" by pushing ahead with a plan to keep the UK aligned with the EU in trade of goods, in a bid to maintain the status quo along the Irish border and limit the damage to the economy.
The Prime Minister told the BBC’s Andrew Marr programme: "I do believe in Brexit. Crucially, I believe in delivering Brexit in a way that respects the vote and delivers on the vote of the British people while also protecting our union, protecting jobs and ensuring we make a success of Brexit for the future."
She said the onus was on the EU to come forward with detailed explanations of its concerns, along with counter-proposals for discussion.
"Chequers at the moment is the only plan on the table that delivers on the Brexit vote and also delivers for the people of Northern Ireland," the Prime Minister told Marr.
"Where they have problems, let's actually hear them and it's only then that you can actually identify what the issue really is, where there are issues that lie behind this.
"My mood is to listen to what the EU have to say about their concerns and to sit down and talk them through with them."
Ms Davidson questioned why the foreign secretary was against a plan for the Irish border that was signed off by the full cabinet in December.
"There's been time over the last two years for debate,” she told the BBC’s Sunday Politics Scotland programme.
"The former foreign secretary was in one of the great offices of state during the time that much of this plan was being constructed - and praised it as soon ago as last year.
"Now is the time for Conservatives to get behind the Prime Minister, give her the space to get the deal done and to back her to deliver for the country.
"In terms of a period of silence, I would be very welcoming of one."
And former Brexit secretary David Davis, who quit Mrs May's Cabinet along with Mr Johnson in protest at the Chequers plan, was dismissive of a series of policy suggestions from the pretender to the Tory leadership.
"I think one of the blights of British politics is politicians having fantastic ideas that cost a fortune and don't do much good," Mr Davis told Sky News's Sophy Ridge On Sunday.
"Boris is a great mate of mine, we have a very knockabout friendship, but quite a lot of his ideas, I think, are good headlines but not necessarily good policies."
"I will vote against Chequers, full stop, and it won't lead to a general election," he said.
"We are capable of managing this through."