Following human occupation, the house mouse has colonised numerous islands, exposing the species to a wide variety of environments. Such a colonisation process, involving successive founder events and bottlenecks, may either promote random evolution or facilitate adaptation, making the relative importance of adaptive and stochastic processes in insular evolution difficult to assess. Here, we jointly analyse genetic and morphometric variation in the house mice (Mus musculus domesticus) from the Orkney archipelago. Genetic analyses, based on mitochondrial DNA and microsatellites, revealed considerable genetic structure within the archipelago, suggestive of a high degree of isolation and long-lasting stability of the insular populations. Morphometric analyses, based on a quantification of the shape of the first upper molar, revealed considerable differentiation compared to Western European populations, and significant geographic structure in Orkney, largely congruent with the pattern of genetic divergence. Morphological diversification in Orkney followed a Brownian motion model of evolution, suggesting a primary role for random drift over adaptation to local environments. Substantial structuring of human populations in Orkney has recently been demonstrated, mirroring the situation found here in house mice. This synanthropic species may thus constitute a bioproxy of human structure and practices even at a very local scale.