Numerous studies have demonstrated population genetic structuring in marine species, yet few have investigated the effect of vertical zonation on gene flow and population structure. Here we use three sympatric, closely related clinid species, Clinus cottoides, C. superciliosus and Muraenoclinus dorsalis, to test whether zonation on South African intertidal rocky shores affects phylogeographic patterns. We show that the high‐shore restricted species has reduced gene flow and considerably higher Fst values (Fst = 0.9) than the mid‐ and low‐shore species (Fst < 0.14). Additionally, we provide evidence for remarkably different demographic and evolutionary histories, ranging from extreme population bottlenecks to population persistence, which are probably linked to effective population size and habitat specialisation. This study further highlights the need for a multispecies approach to unravel the biological and evolutionary processes that drive extant population genetic patterns in marine species, as even closely related species with similar life histories show highly variable results.