He graduated from College of New Jersey (now Princeton University) in 1825 and worked as a lawyer in Freehold.
In 1856, he was the first Republican vice-presidential candidate. During the American Civil War, Dayton served as the United States Ambassador to France. In 1837, he was elected to the New Jersey Legislative Council, then became an associate judge of the New Jersey Supreme Court the following year.
Following the death of United States. Senator Samuel L. Southard he was appointed to the United States Senate starting July 2, 1842, and elected to finish the term ending in 1845.
He was re-elected by the New Jersey Legislature as a Whig in 1845, but lost in 1851, ending his service on March 4, 1851. In 1856, he was selected by the nascent Republican Party as their first nominee for Vice President of the United States over Abraham Lincoln at the Philadelphia Convention.
He and his running mate, John C. Fremont, lost to the Democratic ticket of James Buchanan and John C. Breckinridge. Afterwards, he served as New Jersey Attorney General until 1861, when President Lincoln appointed him Minister to France, serving in that role from 1861–1864 throughout most of the American Civil War.
There, Dayton was part of a successful lobbying campaign to prevent the government of Napoleon III from recognizing the independence of the Confederacy or allowing Confederate use of French ports.
Dayton died in Paris in 1864 while serving in that capacity. He was buried in Riverview Cemetery, Trenton, New Jersey. Later, the town of Dayton, New Jersey was named in his honor.
Whig Party, Republican Party.