Value creation in the circular economy (CE) is a result of co-creation. In the industrial context, the theme of collaboration has been studied extensively on a company-to-company basis, but related public agency remains unexplored. Still, circular actions happen in societal contexts where public actors and logics are constantly present, enabling the change toward more sustainable actions. For systematic discovery of the topic, the following research questions are considered: (a) What roles can a public actor have in an industrial CE ecosystem? (b) What are the relationship modes a public actor can have? (c) In what kind of actor structures may the roles and modes occur? The study relies on two multiple case studies in the international (Study 1) and Finnish eco-industrial parks (Study 2) contexts. The results are based on qualitative content analysis conducted with both primary and secondary data. As a result, six distinct roles—operator, organizer, financer, supporter, policymaker, and regulator—and two modes—facilitative and dirigiste—for public agency in industrial CE ecosystems were identified. The roles depict the concrete means used by public actors whereas the modes depict the characteristics of these actions. Finally, exemplar organization models for the recognized roles and modes in industrial CE ecosystems were examined. The study provides insights into how public actors can contribute to sustainability transitions among their territories and helps practitioners to better understand the premises for public–private interaction.