Redtail shrimp Fenneropenaeus penicillatus are commercially important shrimp species. However, the aquaculture of this species is hindered by insufficient seed supply, mainly caused by frequent inadequate gonad development. The vitellogenin receptor (VgR) plays an important role in the gonad development of oviparous animals by facilitating the accumulation of vitellogenin and nutrients in the oocytes. Therefore, in this study, we cloned and functionally characterized a novel VgR from F. penicillatus (FpVgR). In general, FpVgR has a length of 3795 bp, encoding 1264 amino acid residues and encompassing 28 exons. The calculated molecular weight and theoretical isoelectric point of FpVgR were 139.18 kDa and 4.76, respectively. FpVgR mRNA was highly expressed in the ovary at developmental stages 3 and 4, and localized in the oocyte's plasma membrane. Knocking down FpVgR significantly reduced transcription levels in ovarian tissue, resulting in DNA damage and cell apoptosis within the ovarian tissues. The results of transcriptomic profiling following FpVgR knockdown also revealed that the apoptosis signaling pathway and oxytocin signaling pathway were involved in regulating ovary development and maintaining homeostasis. These findings offer valuable understanding into the mechanisms governing vitellogenesis and the maturation of oocytes, with a specific focus on FpVgR, contributing to future research on vitellogenesis and ovarian development in F. penicillatus.