Genomic analyses may be able to reveal new insights into within-island evolution. Here, genotyping-by-sequencing SNP data were used to analyze genomic variation in the Canary Island gecko Tarentola delalandii from Tenerife and La Palma. We find that ancient within-island divergence events appear to explain genomic variation within Tenerife and likely began some 1.4 – 2.8 Ma ago; considerably more recent than previous estimates from mtDNA sequence divergence. The applications of a more robust rate calibration and multispecies coalescent dating appear to primarily explain these differences. The recent island of La Palma was colonized from northern Tenerife at least ~1 Ma after it appeared, i.e., 0.34-0.75 Ma ago, and after populations had diverged within Tenerife. Admixture analyses revealed that secondary contact (and admixture) among divergent east coast Tenerife populations likely occurred in the late Pleistocene. Some fragmentation events coincide well, spatially and temporally, with ancient mega landslides, such as the Güimar valley collapse, while others do not. The origins of lineages that are spatially associated with the Teno and Anaga shield volcanoes to the NW and NE of the Teide stratovolcano seem to postdate the appearance of these edifices: extinctions due to volcanic eruptions on the central shield volcano appear more likely to explain their genesis. The study provides detailed insights into how biodiversity is generated within a relatively small oceanic island.