N6-methyladenosine (m6A) is a prevalent, reversible chemical modification of functional RNAs and is important for central events in biology. The core m6A writers are Mettl3 and Mettl14, which both contain methyltransferase domains. How Mettl3 and Mettl14 cooperate to catalyze methylation of adenosines has remained elusive. We present crystal structures of the complex of Mettl3/Mettl14 methyltransferase domains in apo form as well as with bound S-adenosylmethionine (SAM) or S-adenosylhomocysteine (SAH) in the catalytic site. We determine that the heterodimeric complex of methyltransferase domains, combined with CCCH motifs, constitutes the minimally required regions for creating m6A modifications in vitro. We also show that Mettl3 is the catalytically active subunit, while Mettl14 plays a structural role critical for substrate recognition. Our model provides a molecular explanation for why certain mutations of Mettl3 and Mettl14 lead to impaired function of the methyltransferase complex. Display omitted •Structures of Mettl3 and Mettl14 complexes show an extensive interface•Crystal structures with bound SAM or SAH identify the active site of Mettl3•Catalytic site of Mettl3, but not Mettl14, is critical for methylation•Mettl14 is critical to support Mettl3 structurally and recognize RNA substrates Wang et al. reveal crystal structures of Mettl3/Mettl14 complexes. Extensive intermolecular contact enables Mettl3 and Mettl14 to work cooperatively. Mettl3 is the catalytic subunit, and Mettl14 activates Mettl3 via allostery and recognition of RNA substrates. They explain why certain mutations, including those involved in cancer, affect RNA methylation.