Rift Valley fever (RVF) virus (RVFV) is an emerging vector-borne pathogen that causes sporadic epizootics and epidemics with multi-year, apparently quiescent, inter-epidemic periods. The epidemiology and ecology of the virus during these inter-epidemic periods is poorly understood. There is evidence for low-level circulation of the virus in livestock and wild ruminants; however, as of yet there is no evidence to identify a specific mammalian reservoir host. Using a systematic approach, this review synthesizes results from serosurveys, attempts at viral detection, and experimental infection of wildlife. These data demonstrate there is a gap in research conducted on RVF in wild ruminants. Specifically, there is very little published data on the pathogenicity of an RVFV infection in various wildlife species, validation of diagnostic assays for exposure to RVFV and understanding of epizootic or endemic disease dynamics in wild ruminants. We recommend that future research on RVFV incorporate a more systematic approach to understand the low-level cycling of the virus during inter-epidemic periods in both wild and domestic ruminant species.