The widespread contamination of pearl farming lagoons in French Polynesia by microplastics has led to questions about risks for the pearl industry. The aim of this study was to test the effects of micro-nanoplastics (MNPs) on the pearl oyster (Pinctada margaritifera) over a 5-month pearl production cycle. MNPs were produced from plastic pearl farming gear and used at a concentration that oysters may encounter in lagoons. MNP exposure led to the alteration of energy metabolism, mostly driven by a lower assimilation efficiency of microalgae, with modulation of gene expression patterns. Pearl biomineralization was impacted by thinner aragonite crystals, with harvest marked by the presence of abnormal biomineral concretions, called keshi pearls. These experimental results demonstrated that MNPs threaten pearl oyster biology, with potential detrimental effects on pearl quality. Ecological approaches are now required to test the holistic impact of MNPs on population sustainability in the Polynesian pearl industry.