Noah’s giant clam (Tridacna noae), recently resurrected from synonymy with T. maxima, occurs from Christmas Island to the Northern Line Islands and from the Ryukyu Islands to New Caledonia. We used mitochondrial and microsatellite markers to investigate the phylogeographic structure and demographic history of T. noae over most of its geographical range. Results from the two types of markers reveal a consistent population structure, partitioning T. noae into three distinct lineages: (1) eastern half of the Indo-Malay archipelago and Western Australia, (2) Melanesia and Micronesia, and (3) Central Polynesia. Demographic expansion initiated between 300,000 and 400,000 years ago was detected for each haplogroup. This pattern, which is congruent with other co-occurring Tridacna species, indicates a shared evolutionary history with expansion from past refuges following late-Pleistocene sea-level changes.