Following his service as governor, Morehead resumed his legal practice in Frankfort, Kentucky. In March 1837, he was commissioned by Governor James Clark to act as an agent for the state, selling bonds to fund internal improvements. He returned to the state House from 1837 to 1838, representing Franklin County. He was president of the Kentucky Board of Internal Improvements from 1838 to 1841, and in 1839, he and John Speed Smith were chosen as commissioners to the state of Ohio to secure the return of Kentucky-owned slaves as property of their masters. They were successful in this endeavor.