Background <p>Growing evidence highlights the importance of epitranscriptomic regulation in cerebellar development and function, especially through m⁶A methylation. Nevertheless, the precise function of the RNA demethylase Fto in the cerebellum is still uncertain.</p> Methods <p>An <i>Fto</i> knockout (<i>Fto</i>^<i>KO</i>) mouse model was generated to investigate the role of <i>Fto</i> in cerebellar development. Cerebellar function was assessed using the behavioral tests and Nissl staining. Immunofluorescence was performed to detect molecular expression levels and subcellular localization. Dot blot, m⁶A-RIP-seq, ATAC-seq and CUT&amp;Tag-seq were used to confirm m⁶A levels and chromatin accessibility. Co-IP was employed to test molecular interactions.</p> Results <p><i>Fto</i>^<i>KO</i> mice exhibited cerebellar ataxia, including tremors and abnormal gait patterns. Reduced FTO expression at embryonic day 13.5 (E13.5) and postnatal day 3 (P3) stages resulted in increased TUJ1 expression, as well as reductions in neuronal functional genes (<i>Map2</i>) and self-renewal genes (<i>Sox2</i>, <i>Sox9</i>, <i>Nestin</i> and <i>Pax6</i>). Mechanistically, <i>Kat8</i> upregulation was linked to the high m⁶A levels regulated by <i>Fto</i> loss. Furthermore, IGF2BP3 specifically recruited acetyltransferase KAT8 to control gene transcription during early cerebellar development by regulating H4K16ac modification, which alters chromatin accessibility in neural developmental pathways.</p> Conclusions <p>In summary, <i>Fto</i>^<i>KO</i>-induced <i>Kat8</i> upregulation in an m⁶A-dependent manner resulted in enhanced KAT8 recruitment by IGF2BP3, which improved chromatin accessibility and H4K16ac modification, thereby promoting cerebellar developmental dysfunction.</p>