The human head louse (Pediculus humanus capitis) is an obligate ectoparasite of humans and has the potential to uncover aspects of human history that cannot be directly inferred from genetic data derived from humans. Previous studies have shown that global louse populations exhibit restricted patterns of genetic variation. However, these studies were restricted both genetically and lacked a global sampling. With the aim of capturing the genetic diversity of head louse populations from around the world, we generated whole genome sequences of human head lice from 43 countries, spanning five continents and Oceania, to determine if louse nuclear diversity mirrors its mitochondrial haplotypes or if population genetic structure, genetic diversity, and population connectivity are associated with geographical regions or host behavior. Here we show that there are five nuclear genetic clusters that are associated with large geographical regions, either at continental or intercontinental levels. High genetic variation was found between African and non-African individuals and the highest genetic diversity was found in samples from sub-Saharan Africa, similar to that of humans. Unlike the mitochondrial clades examined in previous studies, nuclear genetic clusters of lice examined here are highly structured based on geography (continentally and major regions within continents). Results from our genome analyses revealed that host-mediated global dispersal as the likely primary process in shaping diversity and maintaining genetic population boundaries within the nuclear genome of the human head louse.