Sean Harford, Ofsted's director of schools, said ensuring faith schools are preparing young people for life in 'modern Britain' was "one of the most important things".
In a speech to the Association of School and College Leaders annual conference he said all schools must be teaching children a full range of views and not just one religion's opinion.
"Inspecting British values has made life difficult for Ofsted," he said, "nevertheless, we are not shirking this responsibility. It is one of the most important things we are doing".
"I say this because schools, particularly those in mono-cultural areas, are on the frontline of ensuring that our society doesn't become fragmented and divided. We have all seen in recent months what can happen when this frontline is breached.
"All our schools, whether secular or of faith, have a huge responsibility for teaching children and young people about the society in which they live and for promoting understanding, tolerance and respect for others.
"As all of you know, tolerance is predicated on knowledge and understanding, so this is where we are focusing our inspectors' efforts, to ensure that schools promote these important values.
"Our inspectors have had to go into schools serving predominantly Muslim communities in Birmingham and Tower Hamlets, Jewish schools in Hackney, and Christian schools in the North East and say some uncomfortable things about how these institutions were failing to prepare their pupils for life in modern Britain.
"This has been a tough call. But it is absolutely essential, for the reasons I have already mentioned, that we apply the same principles and inspect by the same standards in every school in every part of the country.
"Challenging intolerance - in all its forms - is the right thing for all schools to be doing."
In January Grindon Hall Christian School, in Sunderland, was deemed to be inadequate by Ofsted inspectors who claimed it was not teaching diversity.
In the same month Durham Free School was told it would be closed after a scathing Ofsted report.
Inspectors claimed pupils held prejudiced views of other faiths which were not being challenged by the school.
Both schools have made accusations of bad practice against Ofsted. Durham Free school said inspectors had asked inappropriate questions about gay people.
Mr Harford told the conference these accusations were "lurid smears".
He added: "Occasionally, it can be deeply unpleasant and intimidating. We have seen in recent weeks how some of Her Majesty's Inspectors in the North East have been at the receiving end of some particularly lurid smears and accusations about their professional conduct - some of it emblazoned across the pages of the national press and even repeated on the floor of the House of Commons.
"It's of little consolation to these HMI - obliged to stay silent when their professional integrity is being called into question - that many of these claims fail to stand up to even the most superficial scrutiny.
"It is right that we have a robust complaints process, but the type of mud-slinging and public bad-mouthing of inspectors we have seen recently seems to reflect a tendency on the part of a minority of institutions to deflect attention from their own palpable failure to tackle serious issues - whether that's bullying, poor behaviour, safeguarding or inadequate teaching.
"Those who accuse Ofsted of being too heavy-handed in getting to the root of these matters would no doubt be the first to criticise us if we had failed to uncover these problems when we had the chance."