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Jacob Collamer was born on January 8, 1792, in Troy, New York. He graduated from the University of Vermont, read law, was admitted to the bar in 1813, and became partner to Judge James Barrett. He served four terms in the Vermont House of Representatives and from 1833 until 1842 was assistant judge of the Supreme Court of Vermont. Elected to the U.S. House of Representatives in 1842, he advocated the annexation of Texas, supported the Mexican War and the tariff, and received national recognition for his "Wools and Woolens" speech.

Collamer served as postmaster general under President Zachary Taylor. He became a circuit court judge in Vermont from 1850 to 1854. A conservative anti-slavery Republican, he was elected to the Senate in 1855. Throughout his career in Congress, he concentrated on land and tariff issues. He defended his position even when in the minority, as exemplified in his vigorous minority report as a member of the Committee on Territories, chaired by Stephen Douglas. He was one of two senators who refused to vote for the Crittenden Amendment, which proposed resubmitting the Kansas Constitution to popular vote. He opposed the Reconstruction Plan of President Lincoln, advocating congressional control instead. He had received the presidential nomination from Vermont in 1860 but withdrew after the first ballot.