Context: University-based teacher education programs are increasingly committed to teaching about race and racism, but programs continue to face challenges in preparing justice-oriented educators. Critical scholarship on teaching about race and racism has identified some core concepts that teachers should learn, including an understanding of systemic racism. A deeper understanding of the structure and function of White supremacy as a system, specifically as it operates within teacher education as a social institution, can provide insight about the challenges faced by teacher educators (TEs) who teach about race and racism. Drawing from articulations of the characteristics of White supremacy, the author identifies operant mechanisms of White supremacy in teacher education. Purpose: This article offers a framework for the logic of White supremacy as consisting of three core concepts: (1) the logic of racialized distribution of power; (2) the logic of intentional White ignorance and historical erasure; and (3) the logic of dehumanization of people of color through violence and White cultural hegemony. The study examined the tensions that emerge for teacher educators who aim to teach teachers to disrupt White supremacy but are working from within White supremacist institutions. Research Design: The theoretical framework was used to examine emerging tensions experienced by TEs in a cross-institutional qualitative study that used phenomenological methods. Data were collected from teacher educators across multiple institutions and included interviews, classroom artifacts, and focus groups. Findings: Findings aligned to the White supremacy framework. Tensions related to the racial distribution of power focused on differentiated support for teacher candidates (TCs) of color and navigating moments of racial tension. Tensions related to White ignorance and erasure centered on responding to White students' resistance decentering Whiteness. Finally, tensions related to dehumanization of people of color focused on challenging deficit ideologies. Recommendations: The findings suggest that being open to and conscious of these tensions through critical reflection can be productive for teacher educators. More research is needed that considers the distinct needs of TCs of color and White TCs when learning about race and racism. In addition, further research can apply the logic of White supremacy in cross-institutional studies and continue to engage TEs as participants to explore linkages between interpersonal and institutional effects of White supremacy in other contexts.