Due to his conservative elite position, he became close associate of Muhammad Ali Jinnah, then-President of Muslim League, who appointed him as a member of the executive committee to successfully promote Muslim League' party agenda and program that gained popularity in East Bengal. In 1940–41, Nazimuddin broke away from the coalition led by Premier Fazlul Haq and decided to become a leader of the opposition, leading campaign against Haq's premiership and primarily focused on Bengali nationalism issues. In 1943, Nazimuddin took over the government from Premier Haq when the latter was dismissed by the Governor John Herbert amid controversies surrounding in his political campaigns. During this time, Nazimuddin played a crucial political role for the cause for the separate Muslim homeland, Pakistan. About his role, he was asked about the "Pakistan question" by British Governor Richard Casey in 1945 but he showed very little and no interests in discussing the existence of the movement and reportedly quoting: he did not know what Pakistan means and nobody in Muslim League knew."