This paper addresses the question of which function systemic intermediaries (here called ‘transition brokers’) can fulfil in the regional governance of implementing a circular economy (CE). Empirical research on this issue is scarce. The conclusion, based on a comparative case study of six Dutch regions, is that transition brokers fulfil the function of system orchestration. They can enhance processes of change, build alliances, help create the necessary preconditions, and develop impactful circular initiatives from a neutral standpoint. In a multi-stakeholder setting, transition brokers fulfil a variety of roles, depending on time period, content, and context. Executing these roles requires a number of specific competencies, varying from being entrepreneurially minded to daring to leave one’s comfort zone and being able to get the idea of CE accepted in a variety of businesses and organisations. From interviews held with key transition brokers in the six regions, it transpired that there is a clear division of labour between transition brokers vis-à-vis other key actors, among which the local government is included. These findings allow the design of a new model of regional governance in implementing CE from a system level perspective. It is recommended to perform similar case studies in other countries to generalise the results presented here.