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Nanoscale delivery systems have gained a surge of interest in improving the stability, food compatibility, and bioavailability of essential minerals. Biogenic polyphosphate nanoparticles from microalgae have a great potential to enrich and deliver mineral nutrients. Here, zinc-enriched polyphosphate nanoparticles (ZnPNPs) with a zinc/calcium molar ratio of around 0.2 were obtained from Synechococcus sp. PCC 7002 supplemented with 3.75 mg/L zinc in the growth medium, and displayed small size and anionic nature with a monomer diameter of around 18 nm and a zeta potential of around −36 mV. Zinquin fluorescence measurements unveiled that ZnPNPs were well absorbed and readily incorporated into labile zinc pool by polarized Caco-2 cells in vitro. ZnPNPs showed good resistance to phytate's inhibition on zinc transportation across ligated mouse small intestine ex vivo at the phytate × calcium/zinc molar ratio as seen in baked whole wheat bread, and by treating with NaN3, amiloride, low temperature, chloroquine, and wortmanin, ZnPNPs transportation was found to invoke macropinocytic internalization, lysosomal degradation, and transcytosis. Oral pharmacokinetics and liver and skeletal muscle retention of zinc in rats revealed good in vivo zinc bioavailability of ZnPNPs under high dietary phytate conditions. Overall, ZnPNPs are attractive for zinc supplementation/fortification to populations on phytate-rich diets. [Display omitted] • ZnPNPs were obtained from Synechococcus sp. PCC 7002 by the enrichment of zinc. • ZnPNPs could be well absorbed and readily incorporated into labile cell zinc pool in vitro. • A good resistance to phytate's inhibition on zinc transportation was observed across ligated mouse small intestine ex vivo. • ZnPNPs transportation invoked macropinocytic internalization, lysosomal degradation, and transcytosis. • Oral pharmacokinetics revealed good zinc bioavailability of ZnPNPs against high dietary phytate in vivo. [ABSTRACT FROM AUTHOR]