Symbiosis between insects and bacteria has been established countless times. While it is well known that the symbionts originated from a variety of different bacterial taxa, it is usually difficult to determine their environmental source and a route of their acquisition by the host. In this study, we address this question using a model of Neisseriaceae symbionts in rodent lice. These bacteria established their symbiosis independently with different louse taxa (Polyplax,Hoplopleura,Neohaematopinus), most likely from the same environmental source. We first applied amplicon analysis to screen for candidate source bacterium in the louse environment, that is, three species of rodents (Microtus arvalis,Clethrionomys glareolus, andApodemus flavicollis). The screened samples included rodent fur, skin, spleen, and ectoparasites sampled from the rodents. The amplicon analysis revealed a Neisseriaceae bacterium, closely related to the known louse symbionts. We assembled genome drafts of this environmental bacterium from all three rodent hosts. The sizes of the three drafts converged to a remarkably small size of approximately 1.4 Mbp, which is even smaller than the genomes of the related symbionts. Based on these findings, we propose a hypothetical scenario of the genome evolution during the transition of a free-living bacterium to the member of the rodent fur-associated microbiome and subsequently to the facultative and obligate louse symbionts.