BACKGROUND: There is increasing interest amongst donors in investing in the health sectors of fragile and conflict-affected states, although there is limited research evidence and research funding to support this. Agreeing priority areas is therefore critical. This paper describes an 18-month process to develop a consultative research agenda and questions for health systems research, providing reflections on the process as well as its output. METHODS: After a scoping review had been conducted, primary data was collected from August 2014 to September 2015. Data was collected using a mixture of methods, including an online survey (n = 61), two face-to-face group sessions (one with 11 participants; one with 17), email consultation (n = 18), a webinar (n = 65), and feedback via LinkedIn. Two steering committees of purposively selected experts guided the research process - a core steering committee (n = 10) and broad steering committee (n = 20). The process moved from developing broad topics and lists of research needs to grouping and honing them down into a smaller, prioritised agenda, with specific research questions associated to each topic. RESULTS: An initial list of 146 topics was honed down to 25 research needs through this process, grouped thematically under transition and sustainability, resilience and fragility, gender and equity, accessibility, capacity building, actors and accountability, community, healthcare delivery, health workforce, and health financing. They were not ranked, as all health system areas are interdependent. The research agenda forms a starting point for local contextualisation and is not definitive. CONCLUSIONS: A wide range of stakeholders participated in the different stages of this exercise, which produced a useful starting point for health systems research agenda setting in fragile and conflict-affected states. The process of engagement may have been as valuable for building a community of researchers as the product. It is now important to drive forward the research agenda. Without both a higher profile and deeper focus for this area, there is a real risk that fragile and conflict-affected states will continue to fall behind in global health and development goals.