The movement of human populations has greatly influenced the distributions of human commensals. Patterns of genetic variation in contemporary populations can shed light on their demographic history, including long-range migration events and changes in effective population size. The western house mouse, Mus musculus domesticus, is a human commensal and an outstanding model organism for studying a wide variety of traits and diseases. However, we have few genomic resources for wild mice and only a rudimentary understanding of the demographic history of house mice in Europe. Here, we sequenced 59 whole-genomes of mice collected from England, Scotland, Wales, Guernsey, northern France, Italy, Portugal, and Spain. We combined this dataset with 24 previously published sequences from southern France, Germany, and Iran, and compared patterns of population structure and inferred demographic parameters for house mice in Western Europe to patterns seen in humans. Principal component and phylogenetic analyses identified three genetic clusters in Western European mice. Admixture and f-branch statistics identified historical gene flow between these genetic clusters. Demographic analyses suggest a shared history of population bottlenecks prior to 20,000 years ago. Estimated divergence times between populations of house mice from Western Europe ranged from 1,500 to 5,500 years ago, in general agreement with the zooarchaeological record. These results correspond well with key aspects of contemporary human population structure and the history of migration in Western Europe, highlighting the commensal relationship of this important genetic model.