Significance Highly adapted to deep-sea hot vents, the scaly-foot gastropod Chrysomallon squamiferum is unique among living and extinct animals in possessing an imbricating scale-armor reinforced by iron sulfide nanoparticles. Mechanisms behind its biogenic sulfide synthesis are expected to revolutionize industrial production of metal chalcogenide nanoparticles, but how the gastropod manages such processes remains entirely unknown. Here, using state-of-art microscopy and elemental analyses, we show that the living animal mediates biomineralization of iron sulfide nanoparticles via a channel-like columnar organic matrix that transports sulfur, which then reacts with iron ions diffusing in from the surrounding vent fluid. This allows the snail to make iron sulfide nanoparticles in a dynamic low-temperature environment, opening the potential to significantly reduce the industrial production costs of such particles.