He was admitted to legal practice in 1935 with solicitor firm Alexander Grant, Dickson and Menhennitt, and worked there until his admission to the bar in 1946. A talented litigator, he appeared many times before the High Court of Australia and Privy Council, and was appointed as a Queen's Counsel in 1957. He also remained active in the legal and university communities, serving as Vice-Chair of the Victorian Bar Council and a member of the Executive of the Law Council of Australia, and working as a lecturer and serving on several governing boards at the University of Melbourne. His work with the university saw Menhennitt serve as its Warden of Convocation from 1965 to 1968, and as a member of the University Council from 1968 to 1973.