In 1981, Rutter founded his own choir, the Cambridge Singers, which he conducts and with which he has made many recordings of sacred choral repertoire (including his own works), particularly under his own label Collegium Records. He resides at Hemingford Abbots in Cambridgeshire and frequently conducts many choirs and orchestras around the world.
From 1985 to 1992, Rutter suffered severely from myalgic encephalomyelitis (ME, or chronic fatigue syndrome), which restricted his output; after 1985 he stopped writing music on commission, as he was unable to guarantee meeting deadlines.
Rutter also works as an arranger and editor. As a young man he collaborated with Sir David Willcocks on five volumes of the extraordinarily successful Carols for Choirs anthology series.
He was inducted as a National Patron of Delta Omicron, an international professional music fraternity in 1985. Rutter is also a Vice-President of the Joyful Company of Singers, President of The Bach Choir, and President of the Association of British Choral Directors (ABCD).
The world premiere of Rutter's Requiem (1985), and of his authoritative edition of Fauré's Requiem, took place with the Fox Valley Festival Chorus, in Illinois. In 2002, his setting of Psalm 150, commissioned for the Queen's Golden Jubilee, was performed at the Jubilee thanksgiving service in St Paul's Cathedral, London. Similarly, he was commissioned to write a new anthem, "This is the day", for the Wedding of Prince William and Catherine Middleton in 2011, performed at Westminster Abbey during the service.
Rutter's music is eclectic, showing the influences of the French and English choral traditions of the early 20th century as well as of light music and American classic songwriting. Almost every choral anthem and hymn that he writes has a subsequent orchestral accompaniment in addition to the standard piano/organ accompaniment, using various different instrumentations such as strings only, strings and woodwinds or full orchestra with brass and percussion. Many of his works have also been arranged for concert band with optional chorus.
Despite composing and conducting much religious music, Rutter told the US television programme 60 Minutes in 2003 that he was not a particularly religious man yet still deeply spiritual and inspired by the spirituality of sacred verses and prayers. The main topics considered in the 60 Minutes programme, which was broadcast a week before Christmas 2003, were Rutter's popularity with choral groups in the United States, Britain and other parts of the world and his composition Mass of the Children, written after the sudden death of his son Christopher while a student at Clare College, Cambridge, where Rutter himself had studied.
In a 2009 interview Rutter discussed his understanding of "genius" and its unique ability to transform lives - whether that genius is communicated in the form of music or other media. He likened the purity of music to that of mathematics and connected the two with a reference to the discovery made by the early Greeks that frequencies of harmonic pitches are related by whole-number ratios.
Rutter's music is very popular, particularly in the US. In the UK many hold him in high regard, as illustrated by the following quotation from a review in the London Evening Standard (25 September 2005): "For the infectiousness of his melodic invention and consummate craftsmanship, Rutter has few peers". Sue Lawley referred to Rutter as "the most celebrated and successful composer of carols alive today" and Sean Rafferty heralded Rutter as "a creator of not just carols, but wonderfully great things for the human voice." One British composer, David Arditti, did not regard him as a sufficiently "serious" composer, saying that Rutter is "hard to take seriously, because of the way in which his sheer technical facility or versatility leads to a superficial, unstable crossover style which is neither quite classical nor pop, and which tends towards mawkish sentimentality in his sugarily-harmonised and orchestrated melodies."The Guardian remarked that "it is as a writer of carols that he has really made his mark ... His larger-scale works - particularly the Gloria (1974), Requiem (1985) and Magnificat (1990) - are also well established in the choral repertoire."David Willcocks considered Rutter "the most gifted composer of his generation."
The Piano Collection: A Flower Remembered: arrangements of eight of his most popular choral pieces for solo piano. They were recorded by Wayne Marshall on an album released in July 2020 by Decca Records.