The population genetics of parasitic nematodes is influenced principally by a combination of parasite life history traits and host movement ecology. Strongyloides ratti is a parasitic nematode infecting brown rats (Rattus norvegicus) and has an unusual life cycle featuring an obligate parasitic, asexually reproducing generation and a facultative free-living, sexually reproducing generation. This work aims to interrogate the population genetics of S. ratti and compare this to that of its rat hosts, and to look within the S. ratti genome to determine what the distribution of variable sites reveals about ongoing selection on parasitism as a trait. Strongyloides ratti was a common infection of wild rats in three sampling sites in the Southern UK. The sexual form was not observed despite intensive sampling, suggesting that sexual reproduction is very rare within the sampling sites. DNA extracted from rat faeces was used to conduct a population genetic analysis of wild rats, revealing moderate genetic differentiation among sampling sites. Individual S. ratti were subjected to whole genome sequencing, and the 90 genome sequences produced were used to investigate the parasite’s population genetics. The S. ratti sample was partitioned on the level of sympatric, genetically distinct clades, and these did not correlate with sampling site. It is hypothesised that each of the three largest clades was founded by different parasitic females and has subsequently proliferated asexually, with other clades and individuals deriving from rare sexual reproduction among clades. When looking within genomes, it was observed that genes upregulated in the parasitic adult form were more genetically diverse than the rest of the genome. Further, clusters of genes that are comparatively expanded in Strongyloides spp. and putatively contribute to the parasitic lifestyle were consistently more genetically diverse than directly adjacent flanking regions. This suggests that genes involved in parasitism are under diversifying selection.