This paper evaluates the relevance of the regional public art institution in Ontario as it relates to the contemporary global populist moment. Communities in sparsely populated regions are frequently less exposed to cultural, racial, and class differences, making them potentially more susceptible to the rhetoric of right-wing populism. The regional gallery has an opportunity to introduce affective and agonistic presentations of difference that question and complicate existing hegemonic forces. Drawing on theories of public space from Rosalyn Deutsch, antagonism in relational practice from Claire Bishop, and the educational turn from Janna Graham, this paper finds that public art galleries have the capacity to produce agonistic civic spaces. These agonistic tensions, as articulated by political theorist Chantal Mouffe, put into question current hegemonic forms, encouraging the formation of new counter-subjectivities among audiences. These findings are supported by two case studies: Peterborough’s artist-run centre, Artspace, and Oshawa’s Robert McLaughlin Gallery. Interviews were conducted with the curators of each institution, and several exhibitions and programs were analyzed based on the merits of their agonistic potential.