Sucking lice of the suborder Anoplura are permanent ectoparasites with specific lifestyle and highly derived features. Currently, genomic data are only available for a single species, the human lousePediculus humanus. In this study we present genomes of two distinct lineages, with different host spectra, of a rodent lousePolyplax serrata. Genomes of these ecologically different lineages are closely similar in gene content, display a high level of synteny, but they also differ by a few duplications/translocations and single inversion. Compared toP. humanus, the twoP. serratagenomes are noticeably larger (139 Mbp vs. 111 Mbp) and encode a higher number of genes. Similar toP. humanus, they are significantly reduced in sensory-related categories such as vision and olfaction. Utilizing a genome-wide set of genes, we perform phylogenetic reconstruction and evolutionary dating of theP. serratalineages. Obtained estimates reveal their relatively deep origin (approx. 6.5 Mya), comparable to the time of split between the human and chimpanzee licePediculus humanusandP. schaeffi. This dating supports the view that theP. serratalineages are likely to represent two cryptic species with different host spectra. Historical demographies of the two lineages show glaciation-related population size (Ne) reduction, but recent restoration of Ne was seen only in the less host specific lineage. Together with the louse genomes, we analyze genomes of their bacterial symbiontLegionella polyplacis, and evaluate their potential complementarity in synthesis of amino acids and B vitamins. We show that both systems,Polyplax/LegionellaandPediculus/Riesia, display almost identical patterns, with symbionts involved in synthesis of B vitamins but not amino acids.