Mastomys natalensis is widespread in sub-Saharan Africa and hosts several arenavirus species, including the pathogenic zoonotic Lassa virus in West Africa. Mitochondrial lineages sub-divide the range of M. natalensis and have been associated with cryptic structure within the species. To test specificity of arenaviruses to hosts carrying these lineages, we screened 1772 M. natalensis in a large area of Tanzania where three mitochondrial lineages meet. We detected 52 individuals that were positive for one of three arenaviruses: Gairo, Morogoro and Luna virus. This is the first record of Luna virus in Tanzania. We confirmed the specificity of each arenavirus to a distinct host mitochondrial lineage except for three cases in one locality at the centre of a host hybrid zone. No arenaviruses were detected in a large part of the study area. Morogoro and Gairo virus showed differences in prevalence (Morogoro virus lower than Gairo virus) and in genetic structure (Morogoro virus more structured than Gairo virus). However, both viruses have genetic neighbourhood size estimates of the same order of magnitude as Lassa virus. While differences in arenavirus and/or host evolutionary and ecological dynamics may exist, Tanzanian arenaviruses could be suited to model Lassa virus dynamics in M. natalensis.

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Despite the importance of rodents as agricultural pests and reservoirs of zoonoses, the taxonomy and evolutionary history of many groups is still not sufficiently understood. The genus Mastomys (multimammate mice or rats) comprises abundant and intensively studied rodents, widespread across sub‐Saharan Africa. Here, we used an extensive dataset of mitochondrial DNA markers comprising of nearly 2700 individual sequences from 30 African countries to update the information about the geographical distribution of their genetic diversity. In the next step, we sequenced complete mitogenomes, six nuclear markers, and produced anchored phylogenomic data (355 loci) and, for the first time, sufficiently resolved phylogenetic relationships among all extant Mastomys species and reconstructed their evolutionary history. The results suggest eight species of Mastomys occupying various non‐forested environments. Some species are very widespread (Mastomys natalensis, Mastomys kollmannspergeri, and Mastomys erythroleucus; for the latter we provide first records from Tanzania, thus significantly extending its distribution), while others have their distribution restricted to particular geographical areas (Mastomys coucha in South African region, Mastomys awashensis in Ethiopia, and Mastomys angolensis in Angola and southern DRC) or to particular habitat, that is, wetlands in western (Mastomys huberti) or southwestern (Mastomys shortridgei) Africa. The first split separating M. angolensis (with five pairs of mammae only) from remaining multimammate taxa occurred in mid‐Pliocene, but the most intensive radiation occurred in mid‐Pleistocene and was likely driven by the intensification of climate oscillations. The resolved phylogeny of Mastomys will facilitate their further use as model taxa, for example, in understanding proximate mechanisms of evolution of the multimammate phenotype.