Nutritional disease, persistent food insecurity, ecological devastation, and limited sustainable livelihoods among small and beginning (SB) farmers coexist as unintended consequences of trying to address these challenges separately. Agroecology is useful for holistically understanding a community’s food system dynamics, identifying regime lock-ins, and developing pathways to transition to a sustainable food system. Focusing on two often divergent publics, SB farmers and food-insecure populations, this research answers the questions: What critical agroecological characteristics are lacking in a food system contributing to both limited livelihoods of SB farmers and food-insecure populations? In what ways might the relationships of these two publics be central to an agroecological transition to a regional sustainable food system? We present a case study for the city-region Duluth-Northland, Minnesota, USA, by combining methodological and theoretical insights from participatory action research, agroecology, and sustainability transitions literature. Results include a current state of regional food flows, illuminate the food system’s enabling and inhibitory factors, and highlight opportunities for exercising local agency to transition to a sustainable food system using agroecological principles. This research suggests developing relational spaces where two typically divergent publics can dialogue and build reciprocal relationships to construct new food pathways. Findings also highlight a need to develop a social infrastructure to support SB farmer livelihoods, recognize their contribution to the public good, and simultaneously address multiple dimensions of food insecurity. This study provides preliminary guidance for mobilizing action at the nexus of health and food access, environment, and regenerative agriculture livelihoods.