Food insecurity among northern Inuit communities represents a significant public health challenge that requires immediate and integrated responses. In the Inuvialuit Settlement Region (ISR), in the Northwest Territories (NWT), almost half of households experience some degree of food insecurity (33% moderate, 13% severe), and rates are even higher in Nunavut (35% moderate, 34% severe). Currently, food security issues in the Arctic are being addressed by multiple initiatives at different scales; however, the role that governance and policy plays in fostering or hampering Inuit food security remains under-evaluated. We took a participatory-qualitative approach to investigate how food security governance structures and processes are functioning in Inuit settlement areas, using case studies of the Inuvialuit Settlement Region (ISR) and Nunavut, the latter of which has already developed a food security strategy through significant community consultation. Using 18 semi-structured interviews, we examined the development and implementation of the Nunavut Food Security Strategy (NFSS) and Action Plan to identify challenges and lessons learned, identified governance challenges and opportunities in the current way food policy decisions are made in the ISR, and determined ways to improve governance arrangements to address Inuit food security more effectively at a regional scale. Participants implicated in the NFSS process identified a number of challenges, including high rates of employee turnover, coordinating work with member organizations, and lack of a proper evaluation framework to measure the Strategy’s outcomes. In terms of lessons learned, participants expressed the need to establish clear lines of accountability to achieve desired outcomes, and the importance of sufficient and sustained financial resources and organizational capacity to address food security in a meaningful way. Similar themes were identified in the ISR; however, top-down government decision-making at the territorial level and an absence of meaningful community engagement from program administrators during the conceptualization of food security interventions were specific issues identified in this context. In terms of opportunities for regional-scale food security governance, the Government of Northwest Territories (GNWT) is in the process of developing a Country Food Strategy that will engage with a range of stakeholders to develop a broader selection of country food programing. These findings suggest that food security governance remains a key challenge for Inuit. First, sufficient resources are needed to address food security in a sustained manner. Second, existing and planned food security policies and programs should include an evaluation component to demonstrate greater accountability towards desired outcomes. Finally, findings point to the need to develop new collaborative, integrated, and inclusive food security governance arrangements that take into account local context, needs, and priorities. The NFSS is a useful model for collaborative food security governance from which other Inuit regions can learn and adapt.