Nativism has received recent attention because of its salience in American politics, but it dates back to the early days of the Republic. We show nativist sentiments were established in the citizenship-eligibility requirement for the presidency have since been mirrored in the American public’s preferences outside of the executive. We argue that the inclusion of the natural born citizen clause in the U.S. Constitution helped set in motion public expectations for legislative and judicial office holders. Then, with a novel dataset, we show Americans who were not born in the United States have been severely underrepresented in Congress and on the Supreme Court. Finally, using two conjoint designs, we show candidates for Congress and the Supreme Court who fit a nativist mold are preferred by the public across party lines. Overall, we argue a nativist consensus exists in the public which could exacerbate inequalities of representation within American politics.