Lincoln served briefly as a captain on Ulysses S. Grant's staff in 1865 and was present at the Confederate surrender at Appomattox. After the war he completed his legal training in Chicago and was admitted to the Illinois bar in 1867. He built a corporate practice, representing railroads and other businesses, while generally resisting efforts to turn his father's reputation into a presidential candidacy of his own.

James Garfield appointed him secretary of war in 1881. Lincoln continued under Chester A. Arthur after Garfield's assassination, serving until 1885. His department administered the small peacetime army, military posts, and the continuing conflict over federal policy toward Native peoples in the West. In 1889 Benjamin Harrison appointed him minister to Great Britain. Based in London until 1893, he handled diplomatic relations before returning to his Chicago legal and business interests.

Lincoln had served as counsel to George Pullman's railroad sleeping-car company and became its president after Pullman's death in 1897. He was president until 1911, then chaired the board, linking much of his later working life to the corporation's expansion. His business success financed Hildene, the Vermont home where he spent summers and eventually died in 1926. In 1922 he attended the dedication of the Lincoln Memorial in Washington, appearing publicly as the surviving son of the president whose name he had carried through his separate legal, governmental, and corporate career.