In northern Europe, rodent populations display cyclic density fluctuations, which can be correlated with the human incidence of zoonotic diseases they spread. During density peaks, field voles (Microtus agrestis) become one of the most abundant rodent species in northern Europe, yet little is known of the viruses they host. We screened 709 field voles, trapped from 14 sites over three years, for antibodies against four rodent-borne, potentially zoonotic viruses or virus groups: hantaviruses, lymphocytic choriomeningitis virus (LCMV), Ljungan virus (LV) and orthopoxviruses (OPV). Antibodies against all four viruses were detected. However, seroprevalence of hantaviruses, LV and LCMV was low. OPV antibodies (most likely cowpox) were more common but restricted geographically to southeast Finland. Within these sites, antibody prevalence showed delayed density-dependence in spring and direct density-dependence in fall. Higher seroprevalence was found in spring than fall. These results substantially increase knowledge of the presence and distribution of viruses of field voles in Finland, as well as CPXV infection dynamics.