Zinc (Zn2+) homeostasis is essential for gametogenesis and reproduction, and its deficiency causes infertility. Oocytes contain higher Zn2+ levels than somatic cells, and Zn2+ concentrations in oocytes are far higher than those of other transition metals and increase even more during maturation in preparation for fertilization. Remarkably, it is unknown what transporter(s) or channel(s) mediate Zn2+ influx in oocytes and whether they are expressed uniformly throughout folliculogenesis. Here, we showed that the functional expression of a member of the transient receptor potential family, vanilloid 3, TRPV3, closely follows the dynamics of intracellular Zn2+ during oocyte maturation, raising the prospect that these events may be functionally linked. Using microfluorometry, we monitored in oocytes of Trpv3 null females the expected rise in Zn2+ concentrations during maturation. Surprisingly, Zn2+ levels did not climb, and the overall FluoZin3 signal in Trpv3 null eggs was lower than in control eggs. Electrophysiological recordings showed a large TRPV3 current induced by the agonist 2-APB in WT eggs supplemented with extracellular Zn2+ that was absent in Trpv3 null eggs; TRPV3 showed a clear preference for Zn2+ over Ca2+. Trpv3 null eggs displayed features associated with Zn2+ deficient conditions, such as lower IP3R1 function, abnormal cortical granule distribution, and disturbed cytoskeletal organization with distinct actin nucleation disorders. Notably, Trpv3 null eggs demonstrated undisturbed Zn2+ sparks. Our results suggest that TRPV3 is a pivotal member of the Zn2+ toolkit, mediating Zn2+ intake during maturation. They also indicate that distinct transporters or channels mediate Zn2+ influx throughout folliculogenesis.