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Zearalenone (ZEN), a non-steroidal estrogenic fungal toxin widely present in forage, food, and their ingredients, poses a serious threat to animal and human reproductive health. ZEN also threatens ovine, a major source of human food and breeding stock. However, the mechanisms underlying the impact of ZEN on the in vitro maturation (IVM) of ovine oocytes remain unclear. This study aimed to elucidate these mechanisms using the Smart-seq2 technology. A total of 146 differentially expressed genes were obtained, using Smart-seq2, from sheep oocytes cultured in vitro after ZEN treatment. ZEN treatment inhibited <i>RUNX2</i> and <i>SPP1</i> expression in the PI3K signaling pathway, leading to the downregulation of <i>THBS1</i> and ultimately the downregulation of <i>TNFAIP6</i>; ZEN can also decrease <i>TNFAIP6</i> by reducing <i>PTPRC</i> and <i>ITGAM</i>. Both inhibit in vitro maturation of ovine oocytes and proliferation of cumulus cells by downregulating <i>TNFAIP6</i>. These findings provide data and a theoretical basis for elucidating ZEN’s toxicity mechanisms, screening therapeutic drugs, and reducing ZEN-related losses in the ovine industry.