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How influential could Indigenous peoples be if they had a seat in international governance alongside hegemons such as the United States and Russia? Indigenous peoples advocate for such power, but observers may question whether it would make a difference. This situation exists in the Arctic Council, the major international institution for the Arctic region. The Council is a forum to address regional issues, such as climate change or oil development. It is the only international institution in which Indigenous peoples have formal membership. Their involvement is in ways both populist and a resistance to privilege in international politics. The objective of this research is to understand the atypical influence of Indigenous peoples’ organizations in the Arctic Council. Using process tracing, document analysis, observation and interviews, the finding is that Indigenous peoples’ organizations have increased their influence over Council affairs. Twenty years ago, states did not know how to recognize Indigenous peoples. Today, Indigenous peoples are able to block Council action contrary to their interests, especially when it is necessary to convince only one state to change a decision, or veto a choice. This research illuminates the influence of non-state actors in global governance and the democratization of international relations.