He stood as an independent candidate at the 1923 general election but was not elected.
He was first elected to Dáil Éireann as a National League Party Teachta Dála (TD) for the Donegal constituency at the June 1927 general election.
He did not contest the September 1927 general election.He was elected as a Cumann na nGaedheal TD at the 1932 and 1933 general elections.
At the 1937 general election he was re-elected as a Fine Gael TD for Donegal East.
He was re-elected at each general election until he retired at the 1961 general election.
He served as Leas-Cheann Comhairle (Deputy Chairman) during the 12th Dáil from 1944 to 1948.
McMenamin died on 13 February 1964 in Sandymount, Dublin.His daughter Rosaleen Linehan is a famous stage and screen actress in Ireland.