He was appointed as Deputy Keeper at the V&A in 1945, but moved to become Director and Morley Curator at the Fitzwilliam Museum in Cambridge in 1946, and also a fellow of Trinity College, Cambridge, where he remained until his death in 1966.
He published Elizabethan Miniatures in 1943, and The British School of Miniature Portrait Painters in 1948.
Along with Patrick Trevor-Roper and Peter Wildeblood, Winter gave evidence to the Wolfenden Committee, whose report led in 1967 to the decriminalization of sex between adult male homosexuals.
He gave evidence anonymously as "Mr White".
His testimony to the Committee has been portrayed on-screen in the BBC dramatisation, Consenting Adults.