Bushrod Washington practiced law in Virginia after studying with James Wilson in Philadelphia. He served in the House of Delegates in 1787 and supported ratification of the federal Constitution at Virginia's convention in 1788. His legal practice in Alexandria and Richmond also produced reports of decisions of Virginia's appellate court.

President John Adams appointed him to the United States Supreme Court in 1798. During thirty-one years on the bench he generally supported Chief Justice John Marshall's interpretation of federal authority. Yet he wrote the majority opinion in Ogden v. Saunders in 1827, upholding state insolvency laws in circumstances where Marshall dissented. His duties also required regular travel to hear cases in the federal circuit courts of Pennsylvania and New Jersey.

In Corfield v. Coryell in 1823, Washington discussed the privileges and immunities protected for citizens moving between states, an opinion later cited in debates over the Fourteenth Amendment. Away from court he inherited Mount Vernon under his uncle George Washington's will and continued to hold enslaved people on the estate. He became founding president of the American Colonization Society in 1816, advocating settlement in Africa by free Black Americans. He remained on the Supreme Court until his death in Philadelphia in 1829, combining national judicial service with the management of a Virginia slaveholding estate.