Brookeborough (when he was still Captain Brooke) was a member of a dissident group of Ulster Unionist backbench MPs who campaigned for the removal of Terence O'Neill as Prime Minister of Northern Ireland. When O'Neill finally resigned in April 1969 his successor, Major James Chichester-Clark, brought some of this dissident group into his government. Capt. Brooke was made Parliamentary Secretary at the Ministry of Commerce (1969–1970), and then Parliamentary Secretary at the Department of the Prime Minister (1970–1972). Under Brian Faulkner's premiership, he was Government Chief Whip (1971–1972) and also served in the Cabinet from 1971 as Minister of State in the Ministry of Finance.