It can be challenging to identify the forces that drive speciation in marine environments for organisms that are capable of widespread dispersal because their contemporary distributions often belie the historical processes that were responsible for their initial diversification. In this contribution we explore the likely sequence of events responsible for the radiation of walking sharks in the genus Hemiscyllium using a dated molecular phylogeny. The nine currently recognised species in the genus consist of small, benthic sharks that are restricted to the Indo-Australian Archipelago and show limited dispersal at both juvenile and adult stages. We discuss how major tectonic changes, sea level fluctuations and the unique biology of the species may have influenced speciation in the group, as well as the current distribution of the genus and each of its constituent species. Phylogeographic analysis of the genus combined with biogeographic reconstruction of the region shows a recent radiation during the Miocene and Pliocene, and supports a combination of vicariance and founder modes of speciation mediated by major tectonic, geological and oceanographic historical processes.