The silvertip shark (Carcharhinus albimarginatus) is a reef-associated shark, with an intermittent distribution across the Indo-Pacific Ocean. Owing to global declines, the species is listed as Vulnerable under the International Union of Conservation for Nature Red List. Samples from 152 C. albimarginatus were collected from three locations: Papua New Guinea (PNG), east Australia and Seychelles. Samples were analysed using mitochondrial, microsatellite and double-digest restriction-associated DNA (ddRAD) generated single nucleotide polymorphism markers. As expected across a vast oceanic expanse, no gene flow was identified between south-west Pacific locations and Seychelles for any marker (population differentiation measured using Φ_ST values 0.92–0.98, F_ST values 0.036–0.059). Mitochondrial DNA indicated significant population structuring between PNG and east Australia (Φ_ST = 0.102), but nuclear markers suggested connectivity between these geographically close regions (F_ST = 0.000–0.001). In combination with known telemetry movements for C. albimarginatus, our results suggest stepping-stone patterns of movement between regions is likely driven by reproductive requirements. The use of three distinct marker types in this study has facilitated a powerful genetic description of the population connectivity of C. albimarginatus between the three sampled regions. Importantly, the connectivity described between PNG and east Australia should be used as a guide for managing the south-west Pacific stock of C. albimarginatus.