His pedigree as a French organist was impeccable. His father and two grandfathers were organists and choirmasters, and he was tutored privately by Guilmant in 1898. Dupré studied at the Paris Conservatory (1902-1914) with Vierne, Diémer, and Widor
. He had already given his first organ recital at age 10, had been appointed organist at St. Vivien at 12, and had had his oratorio Le Songe de Jacob performed (in his home) at 15. As a youth he also took long walks with the organ builder Cavaillé-Coll; the two discussed organ construction. In 1914, after already having won conservatory prizes for organ and fugue, he received the Grand Prix de Rome for his cantata Psyché.
In 1920 Dupré gave a series of ten recitals in which he played from memory the complete organ works of J.S. Bach; he had learned the music during World War I, for which he had been found unfit for duty. He toured extensively as a virtuoso, giving as many as 110 recitals in a single trip and making ten tours of the U.S. alone between 1921 and 1948. Dupré celebrated his 1,900th concert in 1953. He frequently improvised fugues and organ symphonies from themes suggested by musicians in the audience; his Symphonie-Passion and Le Chemin de la croix (The Way of the Cross) were first improvised in performance (in Philadelphia and Brussels, respectively) and later notated. His written compositions include a series of 76 chorales, a concerto for organ and orchestra, and two symphonies for solo organ. Dupré also wrote several texts on organ technique and improvisation. All his music has a tonal basis overlaid with high chromaticism. His habit of using chords in rapid bunches was soon picked up by his pupils Alain and Messiaen
Dupré's academic appointments included a professorship at the Paris Conservatory from 1926 (an institution he directed from 1954 to 1956) and oversight of the American Conservatory at Fontainebleau (1947-1954). From 1934 until his death at age 85, he also served as organist (succeeding Widor
) at St. Sulpice.