The nearly neutral theory of molecular evolution predicts that small population size is essential for non-adaptive evolution. Evolution of whole-body left-right reversal in snails is generally a compelling example of non-adaptive speciation, because variants with reversed chirality would suffer from reduced mating opportunities within a population. Despite this reproductive disadvantage, sinistral snail species have repeatedly originated from dextral ancestors in terrestrial pulmonates. Here I show that snail speciation by reversal has been accelerated on oceanic islands. Analysing the global biogeography of 995 genera across 84 stylommatophoran families, I found that the proportion of sinistral snail genera was enhanced in genera endemic to oceanic islands. Oceanic islands are relatively small land masses offering highly fragmented habitats for snails. Thus, the upper limit of population size would probably have been small for a long time there. Oceanic islands may have facilitated the fixation of the non-adaptive allele for speciation by reversal, allowing subsequent ecological divergence of sibling species. This study illustrates the potential role of genetic drift in non-adaptive speciation on oceanic islands.