The western house mouse, , 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 -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 1500 to 5500 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.