The son of impoverished Russian Jewish immigrant parents, Menuhin was born in San Francisco. He played the violin from the age of four, going on to study in Paris with the Romanian violinist-composer Georges Enescu, and touring the United States and Europe in his early teens. He was 16 when, in 1932, he played Elgar's Violin Concerto at the composer's 75th birthday concert. Elgar is said to have cancelled a rehearsal almost immediately with the words, "I can add nothing. It cannot be done better... Let's go to the races instead."

During World War Two Menuhin gave hundreds of concerts for Allied troops, including one at the recently liberated Bergen-Belsen concentration camp. In 1944 he commissioned Bela Bartok's Sonata for Solo Violin, helping to achieve recognition for the composer. In 1947 he was the first Jew to play with the Berlin Symphony Orchestra and conductor Wilhelm Furtwangler, who had been criticized for not opposing Nazism.

In 1959 Menuhin settled in London, and in 1963 opened his celebrated school for gifted children, where famous former pupils include the British virtuoso Nigel Kennedy. He began to concentrate on conducting, and inaugurated several music festivals, including those at Gstaad, Switzerland (1957), and Bath, England (1959). In 1966 he performed with the Indian sitarist Ravi Shankar.

Critics have observed that Menuhin's later career as a violinist did not match up to his earlier brilliance, and that from the 1950s there was a loss of spontaneity and technical reliability in his playing. Menuhin recognized the problem and for a time withdrew from the stage to rebuild his technique. As a teacher, conductor and inspirer, however, he has remained pre-eminent, and his immense achievements in bringing classical music to a wider public have been recognized, as well as his support for many other causes.