Duruflé had the rare distinction of having performed with the finest orchestras of Paris over a period of many years. His first such experience took place on November 14, 1930, at Salle Pleyel in a performance of Carnaval (1892), by Alexander Glazunov, presented by the Orchestre symphonique de Paris with the Russian choirs of Vlassof. Two months later, on January 11, 1931, he played for a performance of Israel in Egypt by George Frideric Handel, given by the Concerts Pasdeloup. In the same year he was the organist for a performance with the Symphonie de la Préfecture de Police, given in the Salle of the former Conservatoire. In 1933 he played the organ for performances of the J. S. Bach Magnificat, BWV 243, and the Messe solennelle of Franz Liszt at the Concerts Pasdeloup. His first appearance as soloist for the Saint-Saëns Symphony No. 3, the Organ Symphony, was with the Orchestre symphonique de Paris on February 5, 1933, at the Salle Pleyel, under the direction of Pierre Monteux.

Duruflé was for many years the house organist for the orchestra of the Paris Conservatoire, the Société des Concerts du Conservatoire. The oldest orchestra in Paris, the Société was long considered the best in the city. Duruflé's first season with the orchestra was in 1939–40, succeeding Georges Jacob, and his first appearance was probably on December 4, 1938, when he would have been needed to play organo ad libitum for the first French performance of Karol Szymanowski's Stabat Mater, and the organ continuo for Bach's Cantata 55: Nun ist das Heil, under the direction of Charles Münch. The first time he was featured as a soloist with the Société was during the war, on December 22, 1941, when he played a repeat performance of the Poulenc Organ Concerto, under Münch's direction.

Duruflé and Marguerite Roesgen-Champion played harpsichords for the Société's performance of Bach's Art of Fugue, BWV 1080, in 1943, under the direction of Münch. In 1946 at the Palais de Chaillot, Duruflé was organist for the orchestra's performance of the Bach Mass in B Minor, BWV 232, with the Choral Amicitia, conducted by Jean Constantinesco. In 1964 the orchestra recorded the Saint-Saëns Symphony No. 3, with Duruflé as the organist under Georges Prêtre at Saint Étienne-du-Mont.