Comparative phylogeography is underpinned by the assumption that sympatrically-distributed taxa will have experienced similar environmental histories, resulting in broadly congruent spatial structuring of phylogenetic lineages, particularly if they inhabit similar niches. However, divergent local conditions, specifically those related to microhabitat, may produce significantly divergent systematic signatures of demographic histories. In the present study, we compare the phylogenetic and population genetic spatial patterns displayed by two species of niche-separated (but sympatrically distributed) Australian funnel web spiders (Mygalomorphae: Hexathelidae). We demonstrate that an apparently minor disparity in habitat niche has led to divergent experiences of a common environmental history in the saproxylic Hadronyche cerberea and the ground-burrowing Atrax sutherlandi. Furthermore, we take a crucial first step in documenting the molecular systematics of a group that has traditionally suffered from a dearth of research interest. (C) 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 805-819.