Wildlife conservation is losing ground in the U.S. for many reasons. The net effect is declines in species and habitat. To address this trend, the wildlife conservation institution (i.e., all customs, practices, organizations and agencies, policies, and laws with respect to wildlife) must adapt to contemporary social–ecological conditions. Adaptation could be supported by clear guidelines reflecting contemporary expectations for wildlife governance. We combine elements of public trust thinking and good governance to produce a broad set of wildlife governance principles. These principles represent guidance for ecologically and socially responsible wildlife conservation. They address persistent, systemic problems and, if adopted, will bring the institution into line with modern expectations for governance of public natural resources. Implementation will require changes in values, objectives, and processes of the wildlife conservation institution. These changes may be difficult, but promise improved wildlife conservation outcomes and increased support for conservation. We introduce challenges and opportunities associated with the principles, and encourage dialogue about them among scientists, practitioners, and other leaders in U.S. wildlife conservation. The principles alone will not change the course of conservation for the better, but may be necessary for such change to occur.