For the remainder of
Lord Brookeborough's premiership, Chichester-Clark remained on the back benches. It was not until 1963, when
Terence O'Neill became
Prime Minister of Northern Ireland, that Chichester-Clark was appointed assistant whip, and a month later when
Bill Craig was promoted to the Ministry of Home Affairs, Chichester-Clark took over as Government Chief Whip. Accounts of the period are that Chichester-Clark enjoyed the Whip's office more than any other he was to subsequently hold in politics. This despite including references to anti O'Neill MP and future
DUP Westminster MP,
Johnny McQuade, and the occasional "good row". From the outset, O'Neill took the unusual decision to allow Chichester-Clark to attend and speak at all cabinet meetings while Chief Whip. Proving a competent parliamentary party administrator, O'Neill added Leader of the House of Commons to Chichester-Clark's duties in October 1966, a promotion that made him a full member of the Cabinet. He was also sworn into the
Privy Council of Northern Ireland in 1966. In 1967, O'Neill sacked his Minister of Agriculture,
Harry West, for ministerial impropriety, and Chichester-Clark was appointed in his place, a position he retained for two quiet years. On 23 April 1969, he resigned from the Cabinet one day prior to a crucial Parliamentary Party meeting, claiming that he disagreed with the Prime Minister's decision to grant universal suffrage in local government elections at that time. He stated that he disagreed not with the principle of one man one vote but with the timing of the decision, having the previous day expressed doubts over the expediency of the measure in Cabinet. It has since been suggested that his resignation was in order to accelerate O'Neill's own resignation, and to improve his own position in the jostling to succeed him. O'Neill "finally walked away" ==Prime minister==