Bottlenose dolphins (Tursiops spp.) are found in waters around Australia, with T. truncatus typically occupying deeper, more oceanic habitat, while T. aduncus occur in shallower, coastal waters. Little is known about the colonization history of T. aduncus along the Western Australian coastline; however, it has been hypothesized that extant populations are the result of an expansion along the coastline originating from a source in the north of Australia. To investigate the history of coastal T. aduncus populations in the area, we generated a genomic SNP dataset using a double-digest restriction-site-associated DNA (ddRAD) sequencing approach. The resulting dataset consisted of 103,201 biallelic SNPs for 112 individuals which were sampled from eleven coastal and two offshore sites between Shark Bay and Cygnet Bay, Western Australia. Our population genomic analyses showed a pattern consistent with the proposed source in the north with significant isolation by distance along the coastline, as well as a reduction in genomic diversity measures along the coastline with Shark Bay showing the most pronounced reduction. Our demographic analysis indicated that the expansion of T. aduncus along the coastline began around the last glacial maximum and progressed southwards with the Shark Bay population being founded only 13 kya. Our results are in line with coastal colonization histories inferred for Tursiops globally, highlighting the ability of delphinids to rapidly colonize novel coastal niches as habitat is released during glacial cycle-related global sea level and temperature changes.