In 1938 and 1939 Duruflé was the soloist for the two premieres of Francis Poulenc's Concerto for organ. The experience brought him into brief contact with the Princess Edmond de Polignac, one of the greatest music patrons of the time. Moreover, the greater popularity of the concerto on this side of the Atlantic has lent a singular importance to Duruflé's having played the premieres, which one critic described as “one of his most important assignments.” But given the rocky course of the concerto's genesis, it is surprising the premieres ever came to pass.

The Princess Edmond de Polignac (1865–1943) was the American heiress to the Singer sewing machine fortune. Born Winnaretta Singer, she had a Paris salon that was the center of artistic and musical life between the wars. She showcased Fauré and Debussy, and commissioned new works from the major composers of her day, including Satie, Ravel, Stravinsky, de Falla, Jean Françaix, Igor Markevitch, and Poulenc. From Poulenc she commissioned two works, the Concerto for two pianos and the Concerto for organ. The princess was herself a pianist and organist, having studied the latter with Eugène Gigout and Nadia Boulanger. Her second husband, Prince Edmond de Polignac, thirty years her senior, was a descendant of the Cardinal Melchior de Polignac.

Beginning in 1933, Nadia Boulanger became the princess's advisor for new commissions and for the concerts presented in her salon. Polignac's commission for an organ concerto was made through Boulanger, in the autumn of 1934, and was originally offered not to Poulenc, but to Jean Françaix. Françaix found himself too busy with other projects and suggested Poulenc, who accepted the commission enthusiastically.

On September 16, 1934, the princess wrote to Poulenc offering him 12,500 francs, half of what he wanted for the commission. In the same month, Boulanger wrote to Poulenc, telling him of her delight about the concerto, hoping to chat with him about “the possibility of writing a work that the princess could eventually play, perhaps with a quartet or piano!”