The church choir in 1890 with Revd. Bligh and Mr. F.W. Dawkins, the organist.

There is no record of when a choir was first formed at St. James's. The first reference to it states that by 1886 the organist was earning £30 and the organ blower £4 15s 6d, while the choir expenses were £14 13s. The summer of 1886 saw the first choir treat for the men, an excursion to Portsmouth. "This was to show the parish’s appreciation of all the voluntary work that they did in uplifting the services." In 1892 the new edition of Hymns Ancient and Modern was adopted by the choir and provided many additional hymns. There were twenty men and eighteen boys in the choir by 1889, and in addition to these, there was a second, or afternoon, choir of twenty boys, which trained them ready for the main choir. There was a practice every Friday evening, “at which the boys are obliged to attend regularly”. The magazine of May 1890 reported: “The Choir mustered well and strong. There were over forty both morning and evening. All of them, with the organist, seemed intent on making the service as good as a large body of voices, well trained and kept together, could make it. Their efforts were very successful, and the anthem was especially well and carefully sung.” Read the article Our Choir. For many years, the adult members of the choir were treated to an annual outing on the river and later joined the Sunday School for their annual trip to the seaside. Read an article, Our Choir.

The church choir in the 1890s with Revd. Job, Mr. Phillips the curate and Mr. Dawkins the organist.

The choir frequently received praise from Revd. Coad Pryor on the quality of their singing. In 1919 he reported that “An innovation will soon take place in the Choir. For some considerable time there has been great difficulty in obtaining Alto voices, it has now been decided, and I very heartily concur, to ask half a dozen ladies to help. I believe Mr. Russe has already secured the services of four, and he will be glad to receive the names of any who are willing to help in this very important branch of the Church Services.”

Revd. and Mrs. Harvey entertained the adult members of the choir in the vicarage and the choir boys were always treated to a summer outing and a winter trip to the pantomine. In 1926 a Choir Festival was held in the church with the choirs of St. James’s, Hampton Parish Church and All Saints Church, Hampton. On Christmas Day, 1928, new Ancient and Modern hymn books were available for the choir. The January edition of the magazine reported: “The supplying of these books was made possible by a generous grant made by the Committee of Hymns Ancient and Modern, to whom we are grateful, by the gift of a sum of money (£2 5s. 9d.) from the old Parochial Socials’ Committee, which, at any rate for the time being, has ceased to function……….”

The church choir in the 1950s with Revd. Brunt.

During 1952 the choir had some new male members and at the same time the two ladies in the choir left. The ladies had given devoted service since the war years, but felt "Now that the choir is approaching full strength again, it is right that this period of service, undertaken 'for the duration', should be brought to a close, and the choir become entirely male again." Four years later there was another request for choir singers with the October Spire reporting: "Surely amongst our parishioners there must be some whose voices are good enough to be used 'in consort' in the service of God. A 'prima donna' type of singer is not required. Provided (1) that you have a reasonable voice; 2) you can read music moderately well; (3) you are willing to practise and attend Services regularly - you can do a wonderfully satisfying job of work."

The Tomkins setting for the Preces, Versicles and Responses at Matins and Evensong was introduced for a time in 1957. The May 1957 edition of the Spire reported: “Just a word about Responses. They are ‘the replies of the Congregation - or Choir representing the Congregation - to the Preces or Versicles intoned by the Priest during the course of the service’. Please note words in bold!” However, these were found to be too difficult for the congregation and so the old familiar settings were re-introduced. Read the article Music and the Choir in our Church. Ten years later a new modern setting by Dr. Moreton was introduced.

During 1959 there must have been more singers around as the April Spire reported: "Owing to the influx of new Treble choristers who passed the recent auditions, there will be a limited number of vacancies for Gentlemen (Tenors and Basses) in the choir. They should possess, in addition to a voice of pleasant quality and unbounded enthusiasm for choral singing on the traditional lines of the English Church, at least a rudimentary acquaintance with the reading of musical notation, although they should not withhold themselves because they may lack complete facility in the art of sight-singing."

The April 1962 Spire reported: "At the Annual Parochial Church Meeting Mr. Sargeant was in fine voice as he delivered an impassioned obligato on choir affairs. The many changes of choir masters - no two alike in their interpretation of music; the revised hymn book; the difficulty of obtaining choirboys to whom the financial side was no longer an inducement and whose voices broke earlier than of yore; not to mention the disconcerting behaviour of the organ which occasionally produces resounding notes when none are pressed on the keyboard; made the choir's task difficult indeed."

The Commission on Worship, in 1963, wanted to know the attitude to the music at St. James’s. The policy of the Commission was that the congregation should be encouraged to take an active part in the worship in church. This meant that the music should be simple enough for the congregation to join in with the choir leading the congregation rather than giving a highly polished concert performance. However the problem was that the congegation did not sing up even for the hymns. The July 1963 Spire reported: "Here it is a matter of confidence. The choir could be expanded, and a section placed at the rear of the church in plain clothes, or even as individuals planted among the rest of the congregation. If a few people in the body of the church sang at top volume, others could soon be induced to join in, with a rapid snow-balling effect." Read the article Music in Church.

Then there were choir shortages again, with the December 1965 Spire reporting: "The choir urgently requires enthusiastic singers to fill the undermentioned vacancies. One of the remarks made by the special Commissioners of the Royal School of Church Music who recently visited us was that we were top-heavy - not that we had too many trebles but rather that they tended to overpower too few contraltos, tenors and basses. May I look forward to having your enquiries? Vacancies: Gentlemen. 2 bass and 2 tenor (any age). Ladies: 3 contralto (any age). Girls: 2 soprano (14 to 18 years of age). Boys: 4 (7 to 12 years of age)."

The church choir in the 1990s with Revd. Leathard and Mrs. Marcella den Boer the organist.

Originally, in 1965, the P.C.C. decided not to have a choir at the Parish Communion service, when the altar was at the chancel steps. However, with the re-ordering of the church and the portable altar being used in 1983, it was thought by many that the choir could be re-introduced. Consequently, there was much discussion around this time about having a choir for the 9.30 a.m. communion as well as for the evensong. "Should we, shouldn't we have one at the morning Parish Communion Service? What, then, is against having a choir to lead and help the congregation - and, during the communion of the people, probably sing an anthem?.........." The discussions continued and there were several magazine articles about this. In the end, though, the status quo obtained until 1993 when the P.C.C. agreed, following consultation with the congregation, that the choir should sing on one Sunday a month at the Parish Communion service. This was subsequently extended so that the choir sang on further Sundays for special festivals or saints days.

The settings of the Communion service by Shephard (his 'Addington' service) and Mathias were alternated for several years. A new musical setting of the Liturgy was composed by Martin Hinckley, a member of the choir, in 2003 and was used for a while, running alongside these, although it was eventually thought to be too demanding for the congregation. Read the articles A New Musical Setting of the Liturgy. In 2008, parts of the Salisbury service by Grayston Ives started to replace Addington. Then in 2010, Martin Hinckley wrote a new setting of the Sanctus and Benedictus to replace that part of the Addington service, as the Salisbury version of this was felt to be too long for the congregation to learn.

St. James's Children's Choir was introduced in 2003, run by a member of the choir. They sang during special services like Christmas, Mothering Sunday and Harvest. In the same year, the choir was invited to sing choral evensong in the Tudor chapel of Sutton's Hospital, Charterhouse, in the City of London, and this has since become an (almost) annual event. Read the article The Choir at Charterhouse. A new tradition was started in 2007 of the choir singing parts of Faure's Requiem during an evening All Souls' Service at which parishoners could remember their lost loved ones. The choir also sang evensong at the beginning of Advent in 2011.