Imogen Holst was brought up in west London and educated at the Froebel Demonstration School and St Paul's Girls' School, where her father was director of music. She worked with Herbert Howells before entering the Royal College of Music (RCM) in 1926 to study composition with George Dyson and Gordon Jacob, harmony and counterpoint with Ralph Vaughan Williams, and conducting with William H. Reed. She won several prizes for composition including the Cobbett Prize for a string quartet (1928).
In 1931 Holst began earning her living as a freelance musician, though her hopes of being a concert pianist were dashed by incipient phlebitis in her left arm.
In April 1939 Holst went to Switzerland to study, and she returned just before the outbreak of war. She served on the Bloomsbury House Refugee Committee, working with musicians from Austria and Germany. In January 1940 she was appointed by Sir Walford Davies to be one of six musicians charged with inspiring and organising musical activities among civilians in rural areas. The scheme, originally funded by the Pilgrim Trust, was taken over by the newly formed Council for the Encouragement of Music and the Arts, forerunner of the Arts Council of Great Britain.
In July 1951 she resumed her freelance career, and in the autumn of 1952 the composer Benjamin Britten asked her to come to Aldeburgh, Suffolk, to help with his opera Gloriana. She had first met him and his partner, the tenor Peter Pears, in the 1940s and they became close friends. She lived in Aldeburgh (in a house designed by architect, H. T. Cadbury-Brown) for the rest of her life, initially working closely with Britten both as his music assistant and for the Aldeburgh Festival, of which she was an artistic director from 1956 to 1977.
In 1953 she arranged for string orchestra William Byrd's keyboard setting of an old Irish tune, Sellinger's Round. This became the basis of the Variations on an Elizabethan Theme, jointly composed by Britten, Lennox Berkeley, Arthur Oldham, Michael Tippett and William Walton. The work was premiered at the 1953 Aldeburgh Festival, in honour of the coronation of Queen Elizabeth II.
In 1963 she published An ABC of Music, an introduction to music theory, which is still in print.
In 1964 Imogen Holst left Aldeburgh to concentrate on recording and editing the music of her father. With composer Colin Matthews she edited scholarly editions of her father's works (including four volumes of facsimiles) and compiled A Thematic Catalogue of Gustav Holst's Music (1974).
She was appointed a fellow of the RCM in 1966, an honorary member of the Royal Academy of Music in 1970 and a Commander of the Order of the British Empire (CBE) in 1975. She received honorary doctorates from the universities of Essex (1968), Exeter (1969), and Leeds (1983).
She died in March 1984, aged 76, and is buried in the churchyard of Saint Peter and Saint Paul's Church in Aldeburgh. Her grave can be found directly behind those of Benjamin Britten and Peter Pears. She never married.
In 2007, Boydell Press published Imogen Holst: A Life in Music, edited by Christopher Grogan and Rosamund Strode, to celebrate the 100th anniversary of her birth.