The extensive fossil record of coiled nautiloids indicates that they comprised a diverse assemblage of species in ancient oceans. Today they are represented by the genera Nautilus Linnaeus, 1758 and Allonautilus Ward and Saunders, 1997, inhabiting reef systems throughout the Indo-Pacific region. Some individual populations of Nautilus show subtle differences in shell morphologies, and these morphological differences may be used to diagnose different species. An alternative view is that these differences are simply geographically localized, morphological variants within the broadly distributed taxon generally referred to as Nautilus pompilius Linnaeus, 1758. Here we present a hypothesis for the phylogeny of present-day Nautilus and Allonautilus using molecular characters from two mitochondrial gene regions, 16S rDNA and Cytochrome Oxidase c subunit I. Populations of N. pompilius in Indonesia (Ambon Strait), the Philippines, Vanuatu (New Hebrides Islands), Papua New Guinea, Carter Reef and Osprey Reef (Great Barrier Reef, Queensland, Australia) and N. macromphalus (Sowerby, 1849) in New Caledonia were surveyed as well as samples of N. repertus (Sowerby, 1849) (Rowley Shoals, Western Australia), N. belauensis (Saunders, 1981) (Palau), and N. stenomphalus (Sowerby, 1849) (Queensland, Australia). The gastropod Crepidula striolata (Menke, 1851) was included as an outgroup. Our results indicate that Nautilus is currently undergoing a period of evolutionary radiation throughout the Indo-Pacific region. The topology of the strict consensus tree suggests that the basal divergence between Nautilus and Allonautilus occurred in the waters surrounding the present-day island of New Guinea and the northern part of the Great Barrier Reef in northeast Australia. This was followed by a migration to the east by the common ancestor of N. macromphalus and the N. pompilius populations in Vanuatu, Fiji, and American Samoa. A subsequent migration to the west led to the founding of populations off the west coast of Australia, the Philippines, Palau, and Indonesia. Our results also indicate that N. macromphalus and A. scrobiculatus are phylogenetic species. However, N. pompilius is a paraphyletic assemblage of populations and does not represent a true phylogenetic species. Divergences within the genus Nautilus appear to be driven by geographic isolation, and we discuss how this may be a result of constraints on dispersal imposed by the ecology of the animals.