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Lassa fever (LF) is a viral hemorrhagic fever that causes high morbidity and severe mortality annually. The disease is endemic to two geographically separate areas within tropical West Africa, one in Nigeria and the second predominantly in Sierra Leone-Guinea-Liberia-Mali. Lassa virus (LASV), the causative agent of the disease, exhibits clear delineation of phylogeography between the endemic areas. In order to characterize the genetic nature of Nigerian–non-Nigerian epidemic split, we performed molecular epidemiological analyses on non-Nigerian isolates (lineage IV as well as lineage V) and their sister group from north-central Nigeria (lineage III). The results showed that adaptive genetic diversification has occurred between these currently circulating clusters in the spread process, and a number of replacement divergences have been fixed between these clusters on the viral RNA-dependent RNA polymerase (L protein). This study highlights the viral L protein could be a determinant factor for the epidemic split. • A genomic epidemiological study was conducted on LASV Nigerian–non-Nigerian split. • Adaptive selection has influenced the Nigerian–non-Nigerian epidemic split of LASV. • The adaptive genetic diversification has occurred on viral protein L. [ABSTRACT FROM AUTHOR]