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Phytophagous beetles, particularly those within the superfamilies Chrysomeloidea and Curculionoidea, constitute one of the most diverse and ecologically significant groups of insect herbivores. Within this group, the subfamily Bruchinae is especially notable for its close association with leguminous plant seeds. As most Bruchinae species do not feed during the adult stage, the timing and regulation of vitellogenesis remain unclear. Previous studies suggest that vitellogenesis may be triggered by volatile organic compounds emitted by host seeds, which promote juvenile hormone (JH) synthesis. This increase in JH is hypothesized to stimulate vitellogenesis, enhance female attractiveness, and ultimately facilitate fertilization and oviposition. To explore this hypothesis, we investigated the external cues regulating reproductive physiology in the capital breeder Zabrotes subfasciatus. Specifically, we examined the effects of host seeds and male presence on oviposition dynamics, fecundity, ovary activation, and the expression of vitellogenic genes (vg and vgR) throughout adult life. Our results show that females initiate vitellogenesis during the final phases of adult development, enabling oviposition to begin as early as the first day after emergence. Oviposition remains at basal levels throughout adult life unless both host seeds and males are present (p < 0.0001). This oviposition pattern is consistent with ovary activation dynamics, which reveal that vitellogenesis peaks early in the oviposition period and is prolonged by the presence of seeds and males (p < 0.05). Notably, vg and vgR gene expression respond differentially to these cues (p < 0.05). We integrate our findings with previous literature to propose a working model for the regulation of oviposition in the Bruchinae beetle Z. subfasciatus.