The study identifies Wilms' tumor 1-associating protein (WTAP) and methyltransferase like 14 (METTL14) as new components of the mammalian N6-methyladenosine (m6A) methyltransferase complex, which is catalyzed by methyltransferase like 3 (METTL3). WTAP interacts with METTL3 and METTL14, and is essential for their localization in nuclear speckles enriched with pre-mRNA processing factors and for their catalytic activity in vivo. WTAP and METTL3 primarily bind to mRNAs containing the consensus m6A motif. Depletion of WTAP or METTL3 reduces RNA binding capability and m6A levels, suggesting that WTAP regulates the recruitment of the m6A methyltransferase complex to mRNA targets. Transcriptomic analyses and PAR-CLIP data show that WTAP and METTL3 regulate gene expression and alternative splicing of genes involved in transcription and RNA processing. Morpholino-mediated knockdown of WTAP and/or METTL3 in zebrafish embryos causes tissue differentiation defects and increased apoptosis. These findings indicate that WTAP functions as a regulatory subunit in the m6A methyltransferase complex and plays a critical role in epitranscriptomic regulation of RNA metabolism.The study identifies Wilms' tumor 1-associating protein (WTAP) and methyltransferase like 14 (METTL14) as new components of the mammalian N6-methyladenosine (m6A) methyltransferase complex, which is catalyzed by methyltransferase like 3 (METTL3). WTAP interacts with METTL3 and METTL14, and is essential for their localization in nuclear speckles enriched with pre-mRNA processing factors and for their catalytic activity in vivo. WTAP and METTL3 primarily bind to mRNAs containing the consensus m6A motif. Depletion of WTAP or METTL3 reduces RNA binding capability and m6A levels, suggesting that WTAP regulates the recruitment of the m6A methyltransferase complex to mRNA targets. Transcriptomic analyses and PAR-CLIP data show that WTAP and METTL3 regulate gene expression and alternative splicing of genes involved in transcription and RNA processing. Morpholino-mediated knockdown of WTAP and/or METTL3 in zebrafish embryos causes tissue differentiation defects and increased apoptosis. These findings indicate that WTAP functions as a regulatory subunit in the m6A methyltransferase complex and plays a critical role in epitranscriptomic regulation of RNA metabolism.