The taxonomic history of Nautilus pompilius Linnaeus, 1758, the most widely distributed species of Nautilus Linnaeus, 1758, is complex, mostly owing to the antiquity of the earliest description by the naturalist Rumphius (Rumpf) in 1705. His account of its habits and illustrations of soft anatomy of specimens from Ambon, Molucca Islands, Indonesia were cited by Linnaeus in his description of N. pompilius. Nevertheless, there is almost no information on Nautilus in Indonesia. Live-caught animals (n = 44) from 150–400 m depth off Ambon provide the first morphologic and genetic details on Nautilus pompilius from the type region, including a recently proposed neotype for the type species. An additional sample (n = 62) obtained from the Sumbawa-Lombok Islands area, Indonesia, 1,500km to the southeast appears identical to those from Ambon. These populations have the largest known mature shells (mean ∼198mm diameter, ∼1,160 g shell plus body weight) of any of the numerous Indo-Pacific occurrences of Nautilus pompilius s.l. presently assigned to this species. Aside from size, few major phenotypic aspects differ from other populations of the species throughout its broad Indo-Pacific range. Data from two mitochondrial DNA gene regions identified a strongly supported clade comprising Ambon, Sumbawa, and Philippines N. pompilius s.s. These new data provide a baseline for evaluating genetic, phenotypic and geographic variation in the broadly distributed species N. pompilius s.l., as well as for establishing taxonomic relationships in populations of living Nautilus, including N. pompilius pompilius Linnaeus, 1758.