This article examines the teaching of collaboration within tertiary education, critiquing the hegemony of a neoliberal mandate. This review of academic literature first identifies the significance of social capital and an intrinsic motivation to collaborate, to theorize how an important and complex graduate attribute (termed here 'collaborative dexterity') might be approached by pedagogy. This leads into a historical analysis of research into higher education, revealing how the instrumentalization of collaboration to enhance the private advantage of learners continues to pervade academia's understanding of collaboration. As higher education transitioned from learning 'through' collaboration to learning 'to' collaborate, extrinsic motivations for collaboration were promoted further through assessment procedures, maintaining a narrow economic-exchange approach to collaboration. These educational practices inhibit the development of collaborative dispositions, foster self-interest and ultimately limit graduates' preparation for the needs of collaborative work environments. Moreover, while educational scholarship has extensively explored why collaboration is important and how it may be assessed, much less consideration has been given to how collaboration might actually be taught within diverse disciplinary areas in tertiary education. This suggests an urgent need for further research into how collaboration is taught within tertiary education, in ways that extend beyond a neoliberal conceptualization of collaboration.