Food policy councils provide a forum to address food systems issues and a platform for coordinated action among multisectoral stakeholders. While diverse in structure, most councils aim to develop democratic and inclusive processes to evaluate, influence, and establish integrated policy and programs for healthy, equitable, and sustainable food systems. The Thunder Bay and Area Food Strategy (TBAFS) is one such example that promotes regional food self-reliance, healthy environments, and thriving economies through the implementation of research, planning, policy, and program development. Despite its success, the TBAFS had no formal engagement from the Indigenous communities that make up almost 13% of Thunder Bay’s population (the highest urban Indigenous population in Canada). Recognizing this gap, in 2016, members of the TBAFS began to develop partnerships with regional Indigenous leaders and organizations to better understand the barriers and opportunities to engagement. The result was the establishment of the Indigenous Food Circle, which aimed to reduce Indigenous food insecurity, increase food self-determination, and establish meaningful relationships with the settler population through food. In this paper, we trace the history of the Indigenous Food Circle. Drawing on theories of decolonization and Indigenous food sovereignty, we argue that the Indigenous Food Circle requires more than simply goodwill from TBAFS members and other allied organizations. It demands confronting our histories and engaging in action that transforms current patterns of relations. It means embracing the discomfort that comes with recognizing the prevalence of settler colonialism and developing respectful and just relationships followed by action. We conclude with some suggestions for continuing this work and the opportunity to experiment with food as a tool for reconciliation and resurgence. See the press release for this article.