John Cotton Smith was born on February 22, 1765, to Cotton Mather Smith and Temperance (Worthington) Smith. He graduated from Yale College in 1783, read law under John Canfield, and was later admitted to the bar in Litchfield County in 1786. On October 29, 1786, he married Margaret Evertson from Amenia New York.

In 1793, Smith was elected as first representative for the town of Sharon to the State General Assembly. He remained as representative until 1800 when he was elected to Congress as a Federalist. By 1806, Smith resigned.

In 1806, Smith was elected as Speaker and served two years, from 1807-08. A year later, in 1809 he was elected member of the upper house. In 1810, he was appointed an associate Judge of the Superior Court and Supreme Court of Errors. ...Smith served as Lieutenant Governor in 1811 and 1812. After the death of Govenor Griswold in 1812, Smither became acting governor. He was elected as the twenty-third Governor of Connecticut in 1813 and served until 1818. He was unsuccessful in a re-election campaign in 1817.

Smith's political career ended, but he was very active in community dealings. He was the first President of the Connecticut Bible Society. He was a Vice-President of the American Colonization Society, which was organized in 1817 and "sought to colonize on the West Coast of Africa all Negroes who could secure legal manumission." In 1826 he became President of the American Board of Commissioners for Foreign Missions but resigned the office in 1841. He served as the President of the American Bible Society from 1831 until his death.
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