"Mr Johnson's remarks also underscore the Muslim Council of Britain's call for an inquiry into Islamophobia in the Conservative Party", the council said on Twitter.
He said he opposed a ban on the face-covering veils, but described them as "absolutely ridiculous" and compared their wearers to rebellious teenagers.
Giving evidence to the Commons Foreign Affairs Committee, Mr Johnson said Nazanin Zaghari-Ratcliffe had been "training journalists" at the time of her arrest, even though she maintained she was on holiday.
She added that the language used by Mr Johnson showed he was "pandering to this Islamaphobic attitude bubbling away in the Conservative Party", which she said she had experienced herself.
Conservative backbench MP Andrew Bridgen said Mr Johnson had raised an important subject in a "light-hearted way".
However, Johnson said he did not support a blanket ban on the face veil in the UK.
But a source close to Mr Johnson - who is a bookie's favourite to succeed Mrs May as PM since he quit her Cabinet in protest at Brexit plans - made clear he was in no mood to back down.
"If you tell me that the burka is oppressive, then I am with you", he said.
'If you say that it is weird and bullying to expect women to cover their faces, then I totally agree - and I would add that I can find no scriptural authority for the practice in the Koran.
Tory peer Sayeeda Hussain Warsi, a former party chair and diplomat, accused Johnson of adopting the "dog-whistle" tactics of right-wing firebrand Steve Bannon, US President Donald Trump's former top aide.
Johnson's comments, in response to Denmark's introduction of a ban on burqas in public places, prompted an angry reaction from Muslim organisations and MPs, who accused him of stoking Islamophobia for political gain.
"A single case of abuse is one too many, and since becoming chairman I have taken a zero-tolerance approach", he said.
"The party chairman, the Prime Minister has the right to take the whip ... that's the thing I'd like to see". "I sincerely hope he doesn't continue to use Muslim women as a convenient political football".
Tell MAMA, an NGO tracking hate crime targeting Muslims in Britain, said in a statement that Johnson's comments "dehumanise" Muslim women.
Some suspected Mr Johnson's burka comments were meant to boost his appeal among right-wing members of the party. "You risk turning people into martyrs, and you risk a general crackdown on any public symbols of religious affiliation, and you may simply make the problem worse", he wrote.
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