"We believe that schools with a religious designation should teach not only their own faith but also an awareness of the tenets of other faiths," they said in a statement with the Department for Education and Skills.
The leaders of nine churches endorsed the principles of the first non-statutory National Framework for Religious Education, published in 2004.
This, they said, helped pupils to develop their knowledge of Christianity and other religions, and should combat prejudice and promote sensitivity to others.
Tony Blair is encouraging faith groups to sponsor schools, and many academies are now backed by religious organisations. But critics have argued that they are potentially divisive.
Keith Porteous Wood, director of the National Secular Society, described the move as a "diversionary tactic".
He said: "This new announcement is merely an effort to counter accusations that single-faith schools are divisive. Simply devoting a few hours to talking about other religions does nothing to stop the real divisiveness of these schools - which comes from separating children on grounds of religion at an early age."
Last year, David Bell, the former chief inspector, caused a furore by saying private Muslim schools were threatening cohesion by not teaching about other cultures.
Ofsted figures showed that 42.5 per cent of evangelical Christian schools were failing in their duty to help pupils appreciate and respect other cultures. In Muslim schools, the figure was 36 per cent.
The announcement came after the BBC was forced to alter a religious education study aid on its website after complaints that it was too evangelical. An item on the corporation's Bitesize revision site attempting to define "good and evil" for GCSE pupils was changed after a secular group branded it misleading.
The study aid said that for Christians the words "good and evil" had special meanings, adding: "God is a power for good, the essence of goodness, and believers become good by becoming closer to him."
It goes on: "Christians believe God allows evil to exist because although he wants us to act according to his rules, he also wants us to have a choice between good and evil, and to choose goodness freely". The aid, aimed at assisting pupils in the run-up to exams, ends: "At the end of the day, God judges us on the way in which we have chosen to lead our lives."
The page prompted a complaint from the Derby branch of the National Secular Society, which said it failed to give an objective overview of religious belief. In a letter to the BBC, the group said: "It implies that people can only be good by believing in God. There is absolutely no excuse to say that evil is a force.
"Children should not be led to think that any blame can be put on an evil persuasion. They have to establish their own responsibility for their actions."