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.

Although 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 offseason when they performed on Cape Cod through mid-1932.

He directed Alfred Lunt and Lynn Fontanne in The Taming of the Shrew and Amphitryon 38 (which he translated from the original French) and appeared with them in Idiot's Delight, his last work as an actor.

The latter part of his career was spent 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.

Windust's final work was the direction of an episode of the Startime television anthology series titled "Dear Arthur" that was taped several days before his death.