Ferroptosis is a form of regulated cell death that is characterized by iron-dependent lipid peroxidation. This process is regulated by specific metabolites, the lipid composition of the cells, and antioxidant mechanisms. Although many regulators of ferroptosis have been identified over the past decade, further exploration of other cellular mechanisms, particularly those originating from non-coding regions, is necessary to develop a thorough understanding of the multifaceted regulatory processes underlying ferroptosis. MicroRNAs (miRNAs) play a crucial role in gene regulation and cellular functions. Through a CRISPR-KO screen, we identified miR-940 as a negative regulator of ferroptosis. Bioinformatics analysis, RNAseq, and proteomics revealed that miR-940 suppresses the expression of ACSL4, LPCAT3, DMT1, and NCOA4. In parallel, it promotes the expression of the ferroptosis gatekeeper GPX4. This gene rewiring reduces levels of redox-active iron and diminishes lipid peroxidation, thereby suppressing ferroptosis. Together, these findings suggest a central role for miR-940 in coordinating the inhibition of ferroptosis, presenting a novel regulatory layer for therapeutic exploration.