We introduced a multilevel model of value shift to describe the changing social context of wildlife conservation. Our model depicts how cultural-level processes driven by modernization (e.g., increased wealth, education, and urbanization) affect changes in individual-level cognition that prompt a shift from domination to mutualism wildlife values. Domination values promote beliefs that wildlife should be used primarily to benefit humans, whereas mutualism values adopt a view that wildlife are part of one's social network and worthy of care and compassion. Such shifts create emergent effects (e.g., new interest groups) and challenges to wildlife management organizations (e.g., increased conflict) and dramatically alter the sociopolitical context of conservation decisions. Although this model is likely applicable to many modernized countries, we tested it with data from a 2017–2018 nationwide survey (mail and email panel) of 43,949 residents in the United States. We conducted hierarchical linear modeling and correlational analysis to examine relationships. Modernization variables had strong state-level effects on domination and mutualism. Higher levels of education, income, and urbanization were associated with higher percentages of mutualists and lower percentages of traditionalists, who have strong domination values. Values affected attitudes toward wildlife management challenges; for example, states with higher proportions of mutualists were less supportive of lethal control of wolves (Canis lupus) and had lower percentages of active hunters, who represent the traditional clientele of state wildlife agencies in the United States. We contend that agencies will need to embrace new strategies to engage and represent a growing segment of the public with mutualism values. Our model merits testing for application in other countries.