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We believe Indigenous teacher education, pre-service and in-service, is an investment in tribal nation building (XXXX, 2020; Brayboy, Solyom, & Castagno, 2014; Castagno, 2021). Applied to teacher apprenticeship and professional development, nation building through teacher education goes beyond individualized achievement metrics (e.g. standardized tests) and requires a concerted effort, overtime, to identify, retain, and strengthen Indigenous educational leaders in a systematic way. Although many scholars have highlighted the importance of training culturally responsive teachers to serve the needs of Indigenous youth, innovations in Indigenous teacher mentorship--pre-service and in-service--is not well developed. This paper explores the power of Indigenous teacher mentorship as essential to address tribal nation building. Drawing from a longitudinal, ethnographic study of an Indigenous teacher education program that serves a predominantly rural, high need region, we examine the basic questions: What do Indigenous mentors uniquely bring to teacher education? In what ways do Indigenous mentors support the development of socially, culturally, linguistically, and place-responsive teachers? Using the theoretical frameworks of TribalCrit (Brayboy, 2005) and situated learning (Lave & Wenger, 1991), findings elucidate the significance of Indigenous mentorship for re-membering and re-claiming Indigenous epistemologies, ontologies, and axiologies in relational and intergenerational learning, practices critical for building strong nations and citizens. Discussion of Indigenous teacher mentorship across geographies challenges researchers, policy makers, and educators to think about what it takes to support teaching that goes beyond the school walls and works in partnership with tribal nations.