<jats:p>Outbreaks of locust plagues result from the long-term accumulation of high-density egg production. The migratory locust,<jats:italic>Locusta migratoria</jats:italic>, displays dramatic differences in the egg-laid number with dependence on population density, while solitarious locusts lay more eggs compared to gregarious ones. However, the regulatory mechanism for the egg-laid number difference is unclear. Herein, we confirm that oosorption plays a crucial role in the regulation of egg number through the comparison of physiological and molecular biological profiles in gregarious and solitarious locusts. We find that gregarious oocytes display a 15% higher oosorption ratio than solitarious ones. Activinβ (<jats:italic>Actβ</jats:italic>) is the most highly upregulated gene in the gregarious terminal oocyte (GTO) compared to solitarious terminal oocyte (STO). Meanwhile,<jats:italic>Actβ</jats:italic>increases sharply from the normal oocyte (N) to resorption body 1 (RB1) stage during oosorption. The knockdown of<jats:italic>Actβ</jats:italic>significantly reduces the oosorption ratio by 13% in gregarious locusts, resulting in an increase in the egg-laid number. Based on bioinformatic prediction and experimental verification, microRNA-34 with three isoforms can target<jats:italic>Actβ</jats:italic>. The microRNAs display higher expression levels in STO than those in GTO and contrasting expression patterns of<jats:italic>Actβ</jats:italic>from the N to RB1 transition. Overexpression of each miR-34 isoform leads to decreased<jats:italic>Actβ</jats:italic>levels and significantly reduces the oosorption ratio in gregarious locusts. In contrast, inhibition of the miR-34 isoforms results in increased<jats:italic>Actβ</jats:italic>levels and eventually elevates the oosorption ratio of solitarious locusts. Our study reports an undescribed mechanism of oosorption through miRNA targeting of a TGFβ ligand and provides new insights into the mechanism of density-dependent reproductive adaption in insects.</jats:p>