RNA modification pathways are often mis-regulated in various typers of cancer, with N6-methyladenosine (m6A) playing a pivotal role in cancer progression and metastasis. Methyltransferase-like 3 (METTL3), a core component of the m6A methyltransferase complex, functions not only as an m6A writer but also promotes tumorigenesis through m6A-independent mechanisms. Here, we show that METTL3 is mislocalized to the cytoplasm in breast cancer tumors from patients, contributing to the oncogenic phenotype. Cytoplasmic METTL3 interacts with EXOC7, a key exocytosis regulator. Additionally, METTL3 regulates m6A-dependent alternative splicing (AS) of EXOC7, promoting the expression of a more aggressive isoform. Silencing METTL3 impairs vesicle trafficking and alters the breast cancer secretome. These effects arenot dependent on its enzymatic activity but instead associated with METTL3-mediated stabilization of EXOC7. Furthermore, knockdown of METTL3 , but not inhibition of its catalytic function, impairs invadopodia formation, collagen matrix invasion, and the generation of focal adhesions , all of which are critical for extracellular matrix degradation and cell invasion. Our findings uncover non-catalytic roles of METTL3 in regulating exocytosis and the cancer secretome, with broader implications for other cancer types.