Quitting as Transport Minister he warned that his government's course on Brexit would leave the United Kingdom "economically weakened with no say in the European Union rules it must follow", with the only other option a "no-deal Brexit" which would "inflict untold damage on our nation".
Arguing Britain was "on the brink of the greatest crisis" since World War Two, he said what was on offer wasn't "anything like what was promised".
Johnson's statement was published after May spent much of the day in France and Belgium, laying wreaths alongside fellow leaders to mark the centenary of the Armistice. Meanwhile, a spokesman for May's office says there will not be a second referendum on Brexit under any circumstances.
Jo Johnson's decision to quit as transport minister saw pro-EU and arch-Brexiteers in the Conservative Party unite to attack the Prime Minister's stance.
Cabinet ministers have been visiting 10 Downing St this week to see details of the government's plan for the "divorce deal" and subsequent trading and customs relationship with the EU. "To do anything less will do grave damage to our democracy".
He added it would be a "democratic travesty" if Britons were not able to go back to the polls to vote on the terms of the deal that may be struck with Brussels. Today there are more problems on the Irish border and the resignation of Jo Johnson.More news: Navy Veteran Killed In Thousand Oaks Shooting Had Survived Las Vegas Shooting
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If a deal is voted down by parliament, the country could be thrust into an uncertain future: leaving abruptly without a deal, the collapse of May's government, an election, or, as some opponents of Brexit hope, a new referendum.
But Mrs May will then have to convince many in her own party, as well as others, she has negotiated a good deal before Britain's planned European Union exit next March.
"If these negotiations have achieved little else, they have at least united us in fraternal dismay".
He described this as "a failure of British statecraft unseen since the Suez crisis" but said even a no-deal Brexit "may well be better than the never-ending purgatory" being put forward by the prime minister.
"Indeed he recently observed that the proposed arrangements were 'substantially worse than staying in the EU.' On that he is unquestionably right". On that he is unquestionably right.
Tory former attorney general Dominic Grieve, who backed Remain in the referendum, told BBC2's Newsnight: "This is a matter when, quite frankly, country comes before party allegiance".
Boundless admiration as ever for my brother Jo.