Endothelial-mesenchymal transition (EndMT) is crucial in atherosclerosis (AS) development, but its molecular mechanisms remain incompletely understood. TNFAIP3 is a crucial negative regulator that plays a central role in inflammatory responses and immune responses by inhibiting the NF-κB signaling pathway. This study aims to investigate the molecular mechanisms by which TNFAIP3 regulates EndMT and the progression of AS, as well as to elucidate the role of METTL3-mediated m6A modification in this process. Through both in vivo and in vitro assays, we analyzed the expression of TNFAIP3 in endothelial cells during AS and EndMT. In vitro, we inhibited TNFAIP3 expression in endothelial cells to observe its impact on EndMT. In vivo, we investigated the effects of endothelial cell-specific TNFAIP3 deficiency on EndMT and AS progression. Furthermore, we investigated whether this process is mediated through the NF-κB/Snail signaling pathway and observed the mitigating effect of inhibiting the NF-κB pathway on ox-LDL-induced EndMT. Finally, we studied the mechanism by which METTL3-mediated m6A modification regulates TNFAIP3 expression in endothelial cells. TNFAIP3 expression is downregulated in endothelial cells during AS and EndMT. Inhibition of TNFAIP3 expression in endothelial cells exacerbated EndMT induced by TGFβ or ox-LDL in vitro. Moreover, endothelial cell-specific deletion of TNFAIP3 increased the expression of mesenchymal markers and exacerbated AS progression. This process is mediated through the NF-κB/Snail signaling pathway. Suppression of the NF-κB pathway alleviated ox-LDL-induced EndMT. Additionally, the reduction in TNFAIP3 expression in endothelial cells is mediated by METTL3/YTHDF2-dependent m6A modification. In AS, the expression of METTL3 is upregulated in endothelial cells, accelerating the degradation of TNFAIP3 mRNA via YTHDF2-dependent m6A modification, thereby downregulating its expression levels. This process activates the NF-κB/Snail signaling pathway, which in turn promotes EndMT. This finding highlights the involvement of epigenetic mechanisms in AS, providing a theoretical basis and potential therapeutic targets for inhibiting EndMT and AS progression.