The state was trying to force them to cede land for the benefit of white settlers, but only the federal government was authorized constitutionally to make treaties with the Native Americans and deal with them officially.

Colquitt was said to be able to make a stump speech, try a court case and plead another at the bar, christen a child, preach a sermon, and marry a couple - all before dinner.

In 1838, after Indian Removal had been underway for several years in Georgia and the Southeast by the federal government, Colquitt was elected as a Whig to the Twenty-sixth Congress, serving from March 4, 1839, to July 21, 1840, when he resigned.

Newly available seats were open in the election, due to the resignations of Julius C. Alford, William Crosby Dawson, and Eugenius A. Nisbet.

In 1842 the Georgia state legislature elected Colquitt as a Democrat to the U.S. Senate; he served from March 4, 1843, until his resignation in February 1848.

He supported the Polk administration in the controversy relative to the Oregon Territory, and was a prominent opponent of the Wilmot Proviso throughout the Mexican–American War.

His second son, Peyton H. Colquitt (1831-1863), also served as a Confederate officer; the colonel was mortally wounded in the Battle of Chickamauga and died two days later.