Hunting can fundamentally alter wildlife population dynamics, but the consequences of hunting on pathogen transmission and evolution remain poorly understood. Here we present a study that leverages a unique landscape-scale experiment coupled with pathogen transmission tracing, network simulation and phylodynamics to provide insights into how hunting shapes viral dynamics in puma (Puma concolor). We show that removing hunting pressure enhances the role of males in transmission, increases the viral population growth rate and the role of evolutionary forces on the pathogen (higher purifying and diversifying selection) compared with when hunting was reinstated. Changes in transmission could be linked to short term social changes as male population increases. These findings are supported through comparison with a region with stable hunting management over the same time period. This study shows that routine wildlife management can have profound impacts on pathogen transmission and evolution not previously considered.