John Christie inherited the country house in 1920. He owned the organ building company of Hill, Norman & Beard Ltd and began to adapt Glyndebourne's 80ft long music into an organ room creating on the largest organs, outside of a cathedral, in the country. Christie's fondness for music led him to hold regular amateur opera evenings in this room and it was at one of these that he met his future wife Audrey Mildmay. She was a professional singer had been engaged to add a touch of professionalism to the proceedings. During their honeymoon attending the Salzburg and Bayreuth festivals, Christie and his wife came up with the idea of bringing professional opera to Glyndebourne. They built a theatre with a 300 seat auditorium and a large orchestra pit. Christie engaged the conductor Fritz Busch and stage director Carl Ebert, both exiles from Nazi Germany and staged the first performance on May 28, 1934.
John Christie's original theatre, built on the side of the house, was enlarged and improved many times after its initial construction and by the early 1990s it included a conglomeration of outbuildings housing restaurants, dressing rooms, storage and other facilities. In 1992 the old theatre hosted its last festival and in 1994 construction of a brand new theatre housing a 1200 seat auditorium at Glyndebourne was completed at a cost of some £34 million, raised through public donations.