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He was assistant organist at Southwark Cathedral from 1923 until 1925. Then he continued his education at Keble College, Oxford. He was music director and organist of the new chapel at Princeton University between 1928 and 1935. During his time in America he learned a lot about organ building and listened to musicians playing baroque music.
He soon became famous for his recitals and radio broadcasts in which he played music using historical performance styles. He gave first performances of pieces by composers such as Darius Milhaud, Paul Hindemith and Arnold Schoenberg. Benjamin Britten invited him every year to perform at the Aldeburgh Festival.
In 1948, he was asked to design an organ for the new Royal Festival Hall. When the organ was first played in 1954 not everyone agreed that it was good, but soon it was realised that it was an excellent instrument for playing music from the Baroque and Classical music periods and it had a big influence on the way that other organs were built.
Downes was Professor of Organ at the Royal College of Music from 1954 to 1975 and was the best known British organ teacher of his day. His students included Gillian Weir and Trevor Pinnock. He made many recordings and wrote a book about organ design.