Past geological and climatological processes shape extant biodiversity. In the Hawaiian Islands these processes have provided the physical environment for a number of extensive adaptive radiations. Yet single species that occur throughout the islands provide some of the best cases for understanding how species respond to the shifting dynamics of the islands in the context of colonization history and associated demographic and adaptive shifts. Here we focus on the Hawaiian happy-face spider, a single color-polymorphic species, and use mitochondrial and nuclear allozyme markers to examine 1) how the mosaic formation of the landscape has dictated population structure, and 2) how cycles of expansion and contraction of the habitat matrix have been associated with demographic shifts, including a ‘quantum shift’ in the genetic basis of the color polymorphism. The results show a marked structure among populations consistent with the age progression of the islands. The finding of low genetic diversity on the youngest site coupled with the very high diversity of haplotypes on the slightly older substrates that are highly dissected by recent volcanism suggest that the mosaic structure of the landscape may play an important role in allowing differentiation of the adaptive color-polymorphism.