We investigated the evolutionary history of the grey reef shark (Carcharhinus amblyrhynchos) in the Indo-Pacific (IP) by harnessing the power of thousands of RAD-seq loci sequenced in 175 individuals across its range. We bring strong evidences of the occurrence of a range expansion (RE) originating close to the Indo-Australian Archipelago (IAA) from which two stepping-stone waves (east and westward) started, colonizing almost the entire IP. Consequently, the demographic history of C. amblyrhynchos is best explained by a meta-population model, for which we estimated a homogenous connectivity throughout its range (Nm~10 per generation) by means of coalescent modeling coupled with an Approximate Bayesian Computation framework. An isolation by distance model further highlights the absence of either genetic barriers or preferential migration corridors, despite the dependency of C. amblyrhynchos from coral reefs occurrence. This is consistent with the long-distance swims observed, suggesting that the strong genetic structure at the IP scale (F_ST~0.56 between its ends) is rather the consequence of its large current distribution. We contrasted these results with those previously obtained for the sympatric but strictly lagoon-associated Carcharhinus melanopterus, a species well known for its restricted dispersal ability. While C. melanopterus exhibits a similar RE dynamic, it is characterized by stronger genetic structure and a non-homogeneous connectivity largely dependent on local coral reefs availability. The comparison between the two species sheds new light on shark evolution, emphasizing the role of IAA as source of biodiversity and of dispersal ability in shaping the extent of population structure and genetic diversity.