There is increasing attention to the importance of healthy and environmentally sustainable food supply and demand but little empirical research exists on how this might be achieved. This study examines the potential for inter-sectoral policy and action to support consumer adoption of healthy and sustainable food behaviours, focusing on three key themes: (1) sectoral understandings of healthy and sustainable food behaviours; (2) modes of governance for inter-sectoral action on healthy and sustainable behaviours; and (3) barriers and enablers to inter-sectoral action. We undertook 29 semi-structured interviews with representatives of key government, food industry and non-government organisations in food-related health and environment sectors in Australia. We found that while definitions of health and sustainability are still diverse and often siloed, the rationale of a combined concept was generally acknowledged. There was also consensus on the need for any action to be inter-sectoral, but diverse views on what such action should entail. The main barriers to inter-sectoral action identified included relationships between food system actors and a lack of organisational attention to the issue. Enablers included political and institutional leadership to drive action as well as sector-specific enablers such as market incentives. Overall a range of governance modes were identified that would potentially create a suite of actions across sectors, as well as opportunities to facilitate their implementation. Drawn together our findings outline a framework for action to move beyond the prevailing focus on individual-level change and develop inter-sectoral action and collaboration to support adoption of healthy and sustainable food behaviours.