Crete (Aegean Sea, Greece), like other Mediterranean islands, has a complex palaeogeographical history, including several cycles of fragmentation into palaeoislands and subsequent reconnection. Here, we use the Cretan trap-door spider Cyrtocarenum cunicularium as a model organism to explore the importance of within-island evolutionary processes, such as palaeogeographic events and climatic changes. We assessed the phylogeny, population clustering and historical demography of 61 specimens with mitochondrial (COI) and nuclear (H3) markers. We investigated the isolation-by-distance and spatial diffusion processes that have shaped their past and current distribution and estimated the effect of niche divergence, using species distribution modelling. Two genetic lineages have continuously been distributed in the west and east part of Crete during the last 2 million years. Their genetic structure is concordant with Crete’s fragmentation into palaeoislands during the Pliocene and additionally affected by the sea-level oscillations and climatic changes due to the Pleistocenic glacial cycles. In central Crete, some evidence of genetic admixture between them was found, which needs to be further explored. According to species distribution modelling, the niche of each lineage corresponds to different environmental parameters, while isolation-by-distance was also detected. The divergence between the ‘West’ and ‘East’ lineages was promoted by palaeogeographical factors but seems to be maintained by the species’ poor dispersal abilities and the local ecological adaptation of each lineage. The case of the Cretan C. cunicularium highlights the additive effect of ecogeographical and behavioural factors in shaping insular biodiversity.