An ecological metaphor can enable transitions towards regenerative circular economies. Yet, this potential remains latent because its conceptual development, which is a prerequisite for its practical operationalization, is in its incipient phase and largely vague. To strengthen its epistemological underpinning, we propose a forward-looking interdisciplinary research agenda which brings together theories, ontological positions, analytical approaches, and strategies of action from ecological economics, panarchy theory, socio-metabolic research, process ecology, environ network theory, the constructal law, nature-based solutions, complexity economics, doughnut economics, regenerative economics, and ergodicity economics. The agenda facilitates the concentration, consolidation, and acceleration of theoretical and methodological innovation for the generation and accumulation of a diverse yet coherent body of knowledge on the interpretation of the process of regeneration and for illuminating the ways in which regenerative circular economies may function.