Paleoarchean jaspilites are used to track ancient ocean chemistry and photoautotrophy because they contain hematite interpreted to have formed following biological oxidation of vent-derived Fe(II) and seawater P-scavenging. However, recent studies have triggered debate about ancient seawater Fe and P deposition. Here, we report greenalite and fluorapatite (FAP) nanoparticles in the oldest, well-preserved jaspilites from the ~3.5-billion-year Dresser Formation, Pilbara Craton, Australia. We argue that both phases are vent plume particles, whereas coexisting hematite is linked to secondary oxidation. Geochemical modeling predicts that hydrothermal alteration of seafloor basalts by anoxic, sulfate-free seawater releases Fe(II) and P that simultaneously precipitate as greenalite and FAP upon venting. The formation, transport, and preservation of FAP nanoparticles indicate that seawater P concentrations were ≥1 to 2 orders of magnitude higher than in modern deepwater. We speculate that Archean seafloor vents were nanoparticle "factories" that, on prebiotic Earth, produced countless Fe(II)- and P-rich templates available for catalysis and biosynthesis.