Indigenous entrepreneurial ecosystem development is not addressed in research. We define and characterise Indigenous entrepreneurial ecosystems and their evolution based on a qualitative study comparing Indigenous entrepreneurship in Chile and in Aotearoa New Zealand. We draw on interviews with 10 Mapuche entrepreneurs in Araucanía and 10 Māori entrepreneurs in the Bay of Plenty, observation, and a literature review to address the question – how does an Indigenous entrepreneurial ecosystem develop along with the social, economic, and political development of mainstream society? We find that Indigenous entrepreneurial ecosystems evolve with the economic and social environments of their countries because of an internal imperative towards cultural continuity and the resilience of culture to change. We find that mature Indigenous entrepreneurial ecosystems are associated with higher states of development and support a broader range of business models. Implications for policy, practice, and research are discussed.