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One of the primary goals in biogeography is to understand how different biotas have been assembled in different regions of the world. The presence of the viviparous sea snakes in the Indian Ocean (IO) poses a unique question in this regard due to their evolutionary origins in Australasia (Australia and New Guinea). Here, we examined the origins and patterns of colonization of the IO sea snake assemblage through time-calibrated molecular phylogenies and ancestral area reconstructions. We further evaluated how past and present barriers to dispersal affect genetic diversity of IO sea snakes by examining the population genetic structure of the widespread sea snake, Hydrophis curtus. Our phylogenetic analyses and ancestral area reconstructions strongly indicate that the majority of the IO sea snakes are derived from the Southeast Asian (SEA) sea snake fauna through dispersal and colonization with an in situ radiation (Hydrophis stricticollis-Hydrophis obscurus clade). Further, many species have undergone vicariant speciation events across the Sunda shelf/Indo-Pacific barrier, which formed during the low sea level periods of the Pleistocene. Population genetic analysis of H. curtus revealed a prominent genetic break between populations broadly distributed in the IO and SEA with limited recent gene flow indicating possible cryptic species. These results suggest that compared to the viviparous sea snake stem group that originated 10.6-6.5 million years ago, the IO viviparous sea snakes have a relatively long and complex evolutionary history in the IO and thus have a unique conservation value.