Exposure to environmental estrogens can disrupt the ovarian endocrine/autocrine/paracrine axis, affecting epigenetic programming and reproductive health. Bisphenol A (BPA), a monomer of polycarbonate plastics and a prototypical endocrine disruptor, has documented effects on ovarian dysfunction; however, its influence on follicular signalling before ovulation remains underexplored. This study investigates BPA's mechanistic influence on zebrafish ovulatory function, focusing on its dual impact as a nuclear progestin receptor (PGR) antagonist and an estrogen receptor (ER) agonist. Results indicate chronic (45 days) BPA exposure at environmentally relevant concentrations (1, 10, 100 μg/L) promotes significant changes in gonadosomatic index (GSI), maturational competence, the yield of ovulated (metaphase II-arrested) eggs and post-ovulatory follicles in BPA-exposed females. Alterations in gonadotropin receptors (fshr, lhcgr), steroidogenic enzyme genes (star, cyp11a1, hsd3b2, p450c17, cyp19a1a, 20β-hsd) and insulin-like growth factors (igf1, igf3) indicate impaired follicular signalling. BPA attenuation of PGR expression in pre-ovulatory follicles aligns with its impeded nuclear translocation, potentially influencing downstream ovulatory gene transcription. Molecular docking analysis indicates a stable BPA-PGR binding, correlating with downregulated ovulatory genes (pla2g4aa, ptgs2a, ptgs2b, ptgesl, and ptger4b), and matrix metalloproteinases (adam8b, adamts9, and mmp9) expression. BPA-exposed follicles fail to mature and ovulate following 17,20β-P (MIS) treatment in vitro, suggesting interference with MIS-PGR interaction. Network toxicology analysis highlights BPA's role in ovulatory dysfunction via the ER/epigenetics/PGR cascade. Finally, BPA-driven disrupted ERα/β homeostasis aligns with alterations in follicular DNA methylation and histone modifications, revealing a global epigenetic shift exacerbating ovarian insufficiency.