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There is an imperative to uncover novel immune regulators that can boost tumour immunogenicity and increase the efficacy of immune checkpoint blockade (ICB) therapy. Epigenetic regulators play critical roles in tumour microenvironment remodelling, and N6\u2010methyladenosine (m<jats:sup>6<\/jats:sup>A) is known to be involved in tumourigenesis. However, the role of m<jats:sup>6<\/jats:sup>A in regulating T\u2010cell function and enhancing anti\u2010tumour immunity remains unexplored.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Several cancer cell lines were treated with STM2457, an enzymatic inhibitor of RNA m<jats:sup>6<\/jats:sup>A methyltransferase METTL3, and explored the transcriptome changes with RNA sequencing (RNA\u2010seq). We then utilised mouse melanoma (B16) and mouse colorectal adenocarcinoma (MC38) models to investigate the effects of METTL3 inhibition on immunotherapy, and analysed the dynamics of the tumour microenvironment via single\u2010cell RNA\u2010seq (scRNA\u2010seq). Furthermore, in vitro and in vivo T\u2010cell cytotoxicity killing assay and CRISPR Cas9\u2010mediated m<jats:sup>6<\/jats:sup>A reader YTHDF1\u20103 knockout in B16 were performed to assess the role and the molecular mechanism of RNA m<jats:sup>6<\/jats:sup>A in tumour killing. Finally, the efficacy of METTL3 inhibition was also tested on human melanoma model (A375) and human T cells.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>We demonstrate that inhibiting METTL3 augments tumour immunogenicity and sustains T\u2010cell function, thereby enhancing responsiveness to ICB therapy. Mechanistically, METTL3 inhibition triggers an interferon response within tumour cells, amplifying the anti\u2010tumour immune response, along with deletion of the m<jats:sup>6<\/jats:sup>A reader protein YTHDF2 in tumours inhibiting major histocompatibility complex (MHC)\u2010I degradation. Remarkably, these anti\u2010tumour effects are reliant on the immune system. Specifically, METTL3 inhibition enhances interferon\u2010gamma (IFN\u03b3) and granzyme B (GzmB) expression, thereby strengthening T\u2010cell killing ability, and concurrently dampening the expression of exhaustion\u2010related genes.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>Targeting METTL3 enhances anti\u2010tumour immunity by boosting T\u2010cell cytotoxicity and reversing T\u2010cell exhaustion. Our study positions METTL3 as an epigenetic checkpoint, highlighting the potential of targeting METTL3 to invigorate intrinsic anti\u2010tumour defenses and overcome immune resistance.<\/jats:p><\/jats:sec><jats:sec><jats:title>Key points<\/jats:title><jats:p><jats:list list-type=\"bullet\">\n<jats:list-item><jats:p>Targeting METTL3 augments tumour cell immunogenicity and sustains T\u2010cell function.<\/jats:p><\/jats:list-item>\n<jats:list-item><jats:p>T cell with METTL3 inhibition can reverse T\u2010cell exhaustion, and promote expression of IFN\u03b3 and GzmB, thereby enhancing cytotoxicity in anti\u2010PD\u20101 therapy.<\/jats:p><\/jats:list-item>\n<jats:list-item><jats:p>YTHDF2 deletion in tumours prolong the lifespan of MHC\u2010I 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