His compositional career has embraced both large and small-scale choral works, orchestral and instrumental pieces, a piano concerto, two children's operas, music for television, and specialist writing for such groups as the Philip Jones Brass Ensemble and the King's Singers. His most recent larger choral works, Requiem (1985), Magnificat (1990) and Psalmfest (1993) have been performed many times in Britain, North America, and a growing number of other countries.

He co-edited four volumes in the Carols for Choirs series with Sir David Willcocks, and, more recently, has edited the first two volumes in the new Oxford Choral Classics series, Opera Choruses (1995) and European Sacred Music (1996).

From 1975 to 1979 he was Director of Music at Clare College, whose choir he directed in a number of broadcasts and recordings.

After giving up the Clare post to allow more time for composition, he formed the Cambridge Singers as a professional chamber choir primarily dedicated to recording, and he now divides his time between composition and conducting. He has guest-conducted or lectured at many concert halls, universities, churches, music festivals, and conferences in Europe, Scandinavia, North America and Australasia.

In 1980 he was made an honorary Fellow of Westminster Choir College, Princeton, and in 1988 a Fellow of the Guild of Church Musicians. In 1996 the Archbishop of Canterbury conferred a Lambeth Doctorate of Music upon him in recognition of his contribution to church music. John Rutter's music is published by Oxford University Press and by Hinshaw Music Inc.