Carter Braxton managed extensive Virginia landholdings and a tobacco business supported by enslaved labor. Representing King William County in the House of Burgesses from 1761, he served on committees concerned with grievances, religion and trade. A moderate critic of imperial policy, he often opposed Patrick Henry's more confrontational methods. During the gunpowder dispute of May 1775 he arranged compensation through his father-in-law Richard Corbin, helping avert a clash between Henry's militia and royal officials.

Virginia sent Braxton to the Continental Congress in 1776. He came to support independence, voted for it in July and signed the Declaration. His constitutional views remained conservative. In An Address to the Convention of the Colony and Ancient Dominion of Virginia he criticized the more democratic proposals associated with John Adams and recommended greater protection for established political leadership. The pamphlet and suspicions about his family connections contributed to his removal from the delegation.

Back in Virginia, Braxton sat in the House of Delegates through most sessions from late 1776 to 1786 and retained influential committee assignments. He later served on the Council of State in 1786–1791 and again from 1794 until his death. Wartime commercial losses, debts and litigation weakened his finances without ending his political influence. He moved to Richmond and continued advising governors and conducting business until 1797, when he died.