Abstract Focal segmental glomerulosclerosis (FSGS) is a common glomerular lesion that manifests as a primary podocyte injury. Multiple genetic risk factors have been reported to be associated with the development of FSGS. However, whether epigenetic factors, especially N6‐methyladenosine (m6A) modifications, are involved in the pathogenesis of FSGS remains unclear. By generating a mouse line with a specific deletion of N6‐adenosine‐methyltransferase‐like 3 ( Mettl3 ) in podocytes ( Mettl3 podko mice), podocytes are isolated and performed RNA‐seq. It is shown that RNA m6A methylation levels are reduced in the renal glomeruli of both animal models and patients with FSGS. A significant decrease in RNA m6A levels in podocytes and the development of an FSGS phenotype are observed in the Mettl3 podko mice. Furthermore, RNA‐seq and m6A‐immunoprecipitated RNA sequencing revealed that silencing Mettl3 expression in podocytes led to a gene expression profile associated with slit diaphragm dysfunction. RNA immunoprecipitation assay and hybridization chain reaction (HCR) analysis further identified the slit diaphragm marker TJP1 as a potential target of Mettl3. Moreover, loss‐ and gain‐of‐function analyses showed that Mettl3 enhances podocyte RNA m6A modification, probably through the TJP1–CDC42 pathway. Finally, treatment of Mettl3 podko and adriamycin (ADR)‐induced FSGS mice with m6A‐mimic compounds markedly ameliorated the progression of FSGS. The findings demonstrate that Mettl3 ‐mediated RNA m6A modification is essential for maintaining podocyte architecture and function and represents a potential therapeutic target for FSGS.