Speciation generates biodiversity, and the mechanisms involved are thought to vary across the tree of life and across environments. For example, well-studied adaptive radiations are thought to be fueled by divergent selection in ecologically variable environments, but additionally are influenced heavily by biogeographic, genomic and demographic factors. Mechanisms of non-adaptive radiations, producing ecologically cryptic taxa, have been less well-studied but should likewise be influenced by these latter factors. Comparing among these contexts can help pinpoint universal mechanisms and outcomes. Here, we investigated the contributions of biogeographic and evolutionary processes to population divergence in Laupala cerasina, a wide-spread endemic on Hawai’i Island and one of 38 ecologically and morphologically cryptic Laupala species. The nine sampled populations showed striking population genetic structure at small spatio-temporal scales, fitting a progression rule pattern where populations have sequentially colonized progressively younger volcanoes on Hawai’i Island. The rapid differentiation among populations and species of Laupala shows that neither a specific geographic context nor ecological opportunity are pre-requisites for rapid divergence. Genomic heterogeneity was strongly dependent on recombination rate and background selection. The genomic landscape was further shaped by elevated divergence in regions harbouring mating song loci in the most recently diverged population pairs. Comparing our findings with recent work on complementary systems supports the influence of mostly universal factors in the speciation process.