METTL3, an RNA methyltransferase involved in mRNA biogenesis and translation control through N6-methyladenosine (m6A) modification, promotes translation of specific mRNAs, including those encoding the epidermal growth factor receptor (EGFR) and Hippo pathway effector TAZ, in human cancer cells. Unlike current models that suggest m6A reader proteins act downstream of nuclear METTL3, this study finds that METTL3 associates with ribosomes and enhances translation in the cytoplasm. METTL3 depletion inhibits translation, and both wild-type and catalytically inactive METTL3 promote translation when tethered to a reporter mRNA. Mechanistically, METTL3 enhances mRNA translation by interacting with the translation initiation machinery. METTL3 expression is elevated in lung adenocarcinoma, and loss- and gain-of-function studies show that METTL3 promotes growth, survival, and invasion of human lung cancer cells. These findings uncover an important role for METTL3 in promoting translation of oncogenes in human lung cancer.METTL3, an RNA methyltransferase involved in mRNA biogenesis and translation control through N6-methyladenosine (m6A) modification, promotes translation of specific mRNAs, including those encoding the epidermal growth factor receptor (EGFR) and Hippo pathway effector TAZ, in human cancer cells. Unlike current models that suggest m6A reader proteins act downstream of nuclear METTL3, this study finds that METTL3 associates with ribosomes and enhances translation in the cytoplasm. METTL3 depletion inhibits translation, and both wild-type and catalytically inactive METTL3 promote translation when tethered to a reporter mRNA. Mechanistically, METTL3 enhances mRNA translation by interacting with the translation initiation machinery. METTL3 expression is elevated in lung adenocarcinoma, and loss- and gain-of-function studies show that METTL3 promotes growth, survival, and invasion of human lung cancer cells. These findings uncover an important role for METTL3 in promoting translation of oncogenes in human lung cancer.