Endometrial receptivity is vital for the successful implantation of embryos in sheep. Insufficient receptivity is a major cause of implantation failure, highlighting the need to understand the underlying mechanisms. MicroRNAs (miRNAs) play an essential role in the epigenetic regulation of endometrial receptivity and embryo implantation by influencing post-transcriptional processes. However, the specific mechanisms by which various miRNAs contribute to endometrial receptivity and embryo implantation in sheep remain to be fully elucidated. Our research highlights the significant role of oar-miR-29a, which promotes the migration and proliferation of sheep endometrial epithelial cells (sEECs). We found that oar-miR-29a enhances mRNA expression associated with proliferation, migration, and epithelial-mesenchymal transition (EMT) in sEECs. Additionally, this miRNA enhances the proliferation and migration capabilities of sheep trophoblast cells (sTCs). Moreover, our findings suggest that the target genes of oar-miR-29a are involved in key biological processes and pathways essential for embryo implantation. Notably, our analysis identifies cell division cycle 42 (CDC42) as a target gene of oar-miR-29a. In summary, oar-miR-29a plays a crucial role in promoting endometrial receptivity by targeting CDC42 in sheep. These findings provide insights into the miRNA-based regulatory mechanisms governing uterine physiology during the early stages of pregnancy, emphasizing the importance of this research for improving reproductive outcomes in sheep.