Planning to become an actor, Windust co-founded with Charles Leatherbee the University Players in 1928 on Cape Cod in Falmouth, Massachusetts. The company lasted five years and included later luminaries Joshua Logan, Henry Fonda, James Stewart, Margaret Sullavan, Mildred Natwick, Eleanor Phelps, Barbara O'Neil, Myron McCormick, Kent Smith, and Aleta Freel. Windust directed more often than he acted. Though he began his association with the Theatre Guild in Manhattan as an assistant stage manager in 1929, he maintained his position as a director of the University Players in the off-season when they performed on Cape Cod through the summer of 1932. Indeed, he quit the Theatre Guild briefly during the winter season of 1931-32 to direct the University Players through its 18-week winter season in Baltimore.
Windust's first major Broadway hit was Life With Father, the Russel Crouse/Howard Lindsay play based on the memoirs of Clarence Day, Jr. , a distant relative on Windust's mother's side. (At 3,224 performances, it held the record for the longest-running Broadway production for many years. ) In quick succession, he followed with Arsenic and Old Lace and Strip for Action, giving him three hits running on Broadway at the same time.
In 1947, Windust relocated to Hollywood, where he worked as the dialogue director on Stallion Road starring Ronald Reagan. His film directing career included two 1948 Bette Davis vehicles, the melodramatic Winter Meeting and the screwball comedy June Bride. The latter part of his career was spent working in the television division of Universal, directing episodes of Alfred Hitchcock Presents, Wagon Train, Leave It to Beaver, and Bachelor Father, in addition to the Thanksgiving 1957 special The Pied Piper of Hamelin, later released as a feature film.