The Foreign Secretary said the speech was a “great statement” and declared: “What matters is the end state and our freedom to do things differently and better.”
He hailed the Prime Minister’s “powerful vision”, which included warnings that a transitional period after the official EU divorce date could last longer than two years.
Mrs May also suggested the European Court of Justice (ECJ) would overrule UK law beyond March 2019.
The plans directly contravene two of the four so-called Brexit “red lines” Mr Johnson revealed to The Sun just days before Tory conference.
The newspaper claimed two of his vetoes were: “The transition period post-Brexit must be a maximum of two years and not a second more”, and that “the UK must refuse to accept new EU or ECJ rulings during transition”.
In her first speech to MPs since a calamitous leader’s speech in Manchester, Mrs May said the transitional period would be longer – “around two years”.
And she revealed the UK “may” remain governed by the ECJ even after the Article 50 deadline has struck.
Liberal Democrats Brexit spokesperson Tom Brake MP responded: “Two of Boris Johnson’s red lines have been scrubbed out, but he is still in the Government causing trouble.
“There is nothing to celebrate just because the Government is tearing itself apart – the Brexit process is still in chaos.”
An Open Britain campaign spokesperson also told Sky News: “Boris Johnson briefs the papers about his Brexit red lines, but it turns out he’s just yellow.
“After weeks of stirring up Cabinet divisions, he caves in the minute conference season is over.
“The only person in this Government weaker than Boris is the Prime Minister, who seems unable to sack him despite his serial disloyalty.”
But Mr Johnson was backed by environment secretary and arch-Brexiteer Michael Gove who tweeted: “Boris is right.”
Strong statement from PM on Brexit – let’s be pragmatic over implementation to secure maximum freedom to diverge from EU in end state
— Michael Gove (@michaelgove) October 9, 2017
Influential backbencher Jacob Rees-Mogg also told Sky News the PM had gone “as far as she could reasonably go” in offering the EU a deal.
“If they reject it, then it would indicate a stubbornness, an obduracy, on their part which would indicate that they probably don’t want a deal,” he said.
While veteran Brexit campaigner Sir Bill Cash added of Mrs May’s speech: “There are a lot of people who are looking very, very carefully at the words.
“The question of whether or not the ECJ would remain fully in control of its jurisdiction over the UK after 31 March 2019 and whether they would continue to make laws in relation to the period after that date is the big question.
“And that is exactly the one question that we have yet to clarify and make absolutely crystal clear what is being said.”