Evolutionary game theory and public goods games offer an important framework to understand cooperation during pandemics. From this perspective, the COVID-19 situation can be conceptualized as a dilemma where people who neglect safety precautions act as free riders, because they get to enjoy the benefits of decreased health risk from others’ compliance with policies despite not contributing to or even undermining public safety themselves. At the same time, humans appear to carry a suite of evolved psychological mechanisms aimed at curbing free riding in order to ensure the continued provision of public goods, which can be leveraged to develop more effective measures to promote compliance with regulations. We also highlight factors beyond free riding that reduce compliance rates, such as the emergence of conspiratorial thinking, which seriously undermine the effectiveness of measures to suppress free riding. Together, the current paper outlines the social dynamics that occur in public goods dilemmas involving the spread of infectious disease, highlights the utility and limits of evolutionary game-theoretic approaches for COVID-19 management, and suggests novel directions based on emerging challenges to cooperation.