Comparative phylogeographical studies in island archipelagos can reveal lineage-specific differential responses to the geological and climatic history. We analysed patterns of genetic diversity in six codistributed lineages of darkling beetles (Tenebrionidae) in the central Aegean archipelago which differ in wing development and habitat preferences. A total of 600 specimens from 30 islands and eight adjacent mainland regions were sequenced for mitochondrial cytochrome oxidase I and nuclear Muscular protein 20. Individual gene genealogies were assessed for the presence of groups that obey an independent coalescent process using a mixed Yule coalescent model. The six focal taxa differed greatly in the number of coalescent groups and depth of lineage subdivision, which was closely mirrored by the degree of geographical structuring. The most severe subdivision at both mitochondrial DNA and nuclear DNA level was found in flightless lineages associated with presumed stable compact-soil habitats (phrygana, maquis), in contrast to sand-obligate lineages inhabiting ephemeral coastal areas that displayed greater homogeneity across the archipelago. A winged lineage, although associated with stable habitats, showed no significant phylogenetic or geographical structuring. Patterns of nucleotide diversity and local genetic differentiation, as measured using PhiST and hierarchical AMOVA, were consistent with high levels of ongoing gene flow in the winged taxon; frequent local extinction and island recolonisation for flightless sand-obligate taxa; and very low gene flow and geographical structure largely defined by the palaeogeographical history of the region in flightless compact-soil taxa. These results show that differences in dispersal rate, mediated by habitat persistence, greatly influence the levels of phylogeographical subdivision in lineages that are otherwise subjected to the same geological events and palaeoclimatic changes.