He condemned the prime minister's decision to move away from a Brexit vision presented in January past year at Lancaster House and towards the Chequers agreement reached earlier this month, which would see the United Kingdom pursue a softer form of Brexit and remain closely aligned with some European Union rules.
"In the 18 months that have followed... a fog of self-doubt has descended", he said, and criticised the government for not presenting the Lancaster House vision to Brussels.
Mr Davies, the Conservative MP for Shipley, said that he had lost trust that the prime minister would deliver Brexit in the wake of her proposals for a compromise forced through at Chequers.
Johnson denounced the plan agreed as a " Brexit in name only" which would leave Britain in a state of "economic vassalage".
Mr Johnson said the question of the Irish border, "which had hitherto been assumed on all sides to be readily soluble" had been allowed "to become so politically charged as to dominate the debate".
The vote also demonstrated the vital importance of the four or five Labour Brexiteers who have repeatedly defied their own party whip and voted with the government.
Johnson resigned as Foreign Secretary last week in protest against Theresa May's Brexit plans, throwing the Cabinet into further chaos and raising the prospect of a leadership challenge against the prime minister.
The Prime Minister was backed by Brexiteer Tory MP David TC Davies, who said it was "high time that Labour MPs, and, yes, some Conservatives, stop the fear-mongering, get behind their country and support the Prime Minister as she leads us out of the European Union".
Brexit supporter Andrea Jenkyns launched the first salvo in an open challenge to her leader, suggesting policies unveiled last week were closer to those who want to remain in the European Union than to those who want to leave.
After avoiding the damaging defeat, the PM now faces a potentially hard session of Prime Minister's Questions and an appearance in front of the Liaison Committee of senior MPs on Wednesday.
While Johnson was delivering his speech May was along the corridor in the Houses of Parliament facing a grilling from a liaison committee, made up of every chair of every House of Commons select committee.
After narrowly escaping defeat in parliament over her plans for leaving the EU, May signalled she would not drop a proposal on Britain's future relationship with bloc - the biggest shift in its foreign and trade policy for nearly half a century.
"We must try now because we will not get another chance to do it right", he said.
"If I can say to her, I know that she wants us to talk about the positives of Brexit and I agree with her, we should be talking about the positive future for this country". We have time in these negotiations.
Showing how tight the numbers are, the government suffered an unexpected defeat on a separate amendment, which will now require it to seek continued participation in the European medicines regulatory framework.
She will also address a group of her backbench MPs this evening.
Geraint Thomas attacks, takes Tour de France lead ahead of Chris Froome
For me, whatever happens now it is a super successful Tour. I committed, got across to Dumoulin and then sat on. I think it's fantastic for us to have those options.