Morton was elected, as a Republican, to the 46th and 47th Congresses representing Manhattan. He served from March 4, 1879, until his resignation, effective March 21, 1881. The 1880 Republican presidential nominee, James A. Garfield, asked Morton to be his vice presidential running mate, attempting to win over disappointed supporters of Ulysses S. Grant's candidacy for a third term. Morton was loyal to Senator Roscoe Conkling, who was Grant's campaign manager; unhappy that Grant had not been nominated, Conkling advised Morton to decline; Morton followed Conkling's advice. Garfield's supporters then turned to Chester A. Arthur, another Conkling supporter. Conkling advised Arthur to decline, but Arthur accepted; Garfield and he were narrowly elected over their Democratic opponents.