Two of his many film appearances were alongside Basil Radford and Naunton Wayne - in Millions Like Us 1943 and in 1949's Passport to Pimlico. In Millions Like Us he appeared in an uncredited role as 'the man on the pier', whilst in Passport To Pimlico he played the part of Frank Huggins.
Other films that John Slater appeared in include Pimpernel Smith 1941, Gert and Daisy's Weekend 1942, Unpublished Story 1942, A Canterbury Tale 1944, For Those In Peril 1944, Against The Wind 1948 and The Silk Noose 1948.