The university said this week that a new course will run from September 2007.
Applications to teach RE in secondary schools are up 40 per cent this year compared to 2005.
Oxford's educational studies department, which dropped RE in 1980, will reinstate its teacher-training course in a move which reflects growing interest in the subject nationwide.
Professor Brian Gates, chairman of the RE Council of England and Wales, welcomed the move, saying: "Although overall secondary pupil numbers are falling, RE has the highest proportion of lessons taught by non-specialist teachers and therefore the need for more, rather than fewer, newly trained specialists is vital for the future health of RE."
Oxford will run the course in association with the Culham institute, an endowed educational trust set up in Oxford to support RE. The course will emphasise the crossover between RE and citizenship. RE is the fastest-growing subject at GCSE and A-level. Nearly 60 per cent of pupils now take a full or short course GCSE.
Last year the Training and Development Agency for Schools announced a "golden hello" for would-be RE teachers.