This study focuses on manifestations of racism and colonialism in teacher education. I build on the theoretical framing of Critical Race Theory and decolonization in order to expose racist and colonial assumptions at the core of teacher education. I highlight in particular the work of covert racism under the cloak of teachers’ professionalism. I focus on what I call ‘professional microaggressions’: subtle forms of racism and colonialism hidden beneath professional definitions. By interviewing graduates of a well-established Indigenous teacher education program in British Columbia, Canada, I examine the mechanisms that still hinder the success of Indigenous teacher candidates in teacher education and in the school system. The study highlights the resilience, resistance, and strategic planning that Indigenous teachers use to challenge the system while advancing their position within it. Lastly, I suggest ways to support Indigenous teacher candidates in teacher education.