Some form of racial literacy is essential for enacting teachers’ personal and professional commitment to embedding Aboriginal and Torres Strait Islander perspectives and knowledges in education. Our experiences of teaching Indigenous education in universities over the last 30 years provide insights into how racial literacy has (and has not) infiltrated teacher preparation degrees in Australian universities. We discuss in a conversational style critical race theorists who have shaped our conceptualisations of research and teaching practice and share our ideas of forms of racial literacy in praxis, even though it is rarely called that, in the field of Indigenous Studies at two universities. We identify through lived examples of teachers of critical Indigenous studies the precedents, enablers, and barriers to sector-wide commitment to graduating racially literate teachers with the intention to illustrate and provoke accountability from those working in university teacher education in advancing a racially just society.