Capacity development is crucial for enduring conservation success. Recent scholarship has called for a systems perspective based on input from local stakeholders to better understand and develop conservation capacity. However, few studies have adopted such an approach to explore interactions among capacities or how capacity development needs and priorities evolve. We address this gap through a case study from Bhutan, centred on perceptions from 52 local conservation practitioners, planners, funders and community members. We use mixed methods to identify which capacities have been important for conservation success, which capacities are needed for future success, which capacities are foundational and how capacities interact. We find that capacity needs have shifted from individual-level knowledge and skills to community- and societal-level capacities in response to changing political and economic dynamics. Participants identified political support and leadership, reliable and sufficient funding, strengthening the research base, and increasing community awareness and engagement as critical future needs. Investing in these capacities holds the promise of further augmenting capacity development, thus increasing the value of limited resources. Our results demonstrate that capacity development should be viewed as a dynamic process and supported by strategic investment even in countries with track records of conservation success.