Paddy fields are hotspots of microbial denitrification, which is typically linked to the oxidation of electron donors such as methane (CH₄) under anoxic and hypoxic conditions. While several anaerobic methanotrophs can facilitate denitrification intracellularly, whether and how aerobic CH₄ oxidation couples with denitrification in hypoxic paddy fields remains virtually unknown. Here we combine a ~3300 km field study across main rice-producing areas of China and ¹³CH₄-DNA-stable isotope probing (SIP) experiments to investigate the role of soil aerobic CH₄ oxidation in supporting denitrification. Our results reveal positive relationships between CH₄ oxidation and denitrification activities and genes across various climatic regions. Microcosm experiments confirm that CH₄ and methanotroph addition promote gene expression involved in denitrification and increase nitrous oxide emissions. Moreover, ¹³CH₄-DNA-SIP analyses identify over 70 phylotypes harboring genes associated with denitrification and assimilating ¹³C, which are mostly belonged to Rubrivivax, Magnetospirillum, and Bradyrhizobium. Combined analyses of ¹³C-metagenome-assembled genomes and ¹³C-metabolomics highlight the importance of intermediates such as acetate, propionate and lactate, released during aerobic CH₄ oxidation, for the coupling of CH₄ oxidation with denitrification. Our work identifies key microbial taxa and pathways driving coupled aerobic CH₄ oxidation and denitrification, with important implications for nitrogen management and greenhouse gas regulation in agroecosystems.