Rodent gammaherpesviruses have become important models for understanding human herpesvirus diseases. In particular, interactions between murid herpesvirus 4 and Mus musculus (a non-natural host species) have been extensively studied under controlled laboratory conditions. However, several fundamental aspects of murine gammaherpesvirus biology are not well understood, including how these viruses are transmitted from host to host, and their impacts on host fitness under natural conditions. Here, we investigate the epidemiology of a gammaherpesvirus in free-living wood mice (Apodemus sylvaticus) and bank voles (Myodes glareolus) in a 2-year longitudinal study. Wood mouse herpesvirus (WMHV) was the only herpesvirus detected and occurred frequently in wood mice and also less commonly in bank voles. Strikingly, WMHV infection probability was highest in reproductively active, heavy male mice. Infection risk also showed a repeatable seasonal pattern, peaking in spring and declining through the summer. We show that this seasonal decline can be at least partly attributed to reduced recapture of WMHV-infected adults. These results suggest that male reproductive behaviours could provide an important natural route of transmission for these viruses. They also suggest that gammaherpesvirus infection may have significant detrimental effects in wild hosts, questioning the view that these viruses have limited impacts in natural, co-evolved host species.