Changes in land use have a major effect on patterns of biodiversity. However, few studies have examined the demographic and genetic shifts associated with a return to semi-natural habitat following extended periods of human disturbance. Here we examine patterns of population structure in a spider restricted to the Pacific coastal strip of North America that exhibits an exuberant colour polymorphism. We use mitochondrial DNA and AFLP markers to examine genetic structure and estimate gene flow. The results show contrasting, gender-specific patterns between these markers that suggest limited dispersal, combined with area effects most likely caused by expansion from refugial habitat patches following land-management changes in a region of the San Francisco East Bay. Colour-morph frequencies are not correlated with this complex genetic structure. Thus, unlike the classical area effects that were based on colour morphs, we demonstrate in T. californicum signals of historical contingency at neutral loci but not at the Colour locus, where traces of past events have been obliterated by balancing selection. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 600–620.