After his initial term as governor, Polk was again elected to the State Senate in 1834, and served in the 1835/36 session as Speaker. As the governor’s constitutional successor, he became governor again upon the death of Governor Caleb P. Bennett and served the remaining months of Bennett's term from July 11, 1836 until January 17, 1837. Polk then returned to his seat in the State Senate, served in the 1837/38 session, and was reelected for the 1839/40 and 1841/42 sessions. He was once again Speaker in the 1841/42 session.