Seagrass meadows are key blue carbon (C) ecosystems, storing large amounts of organic C over centuries. Their climate benefits may be reduced by methane (CH4) emissions, whose microbial and environmental descriptors in Zostera noltei meadows, dominant seagrass in North Western Europe, remain poorly understood. We studied CH4 fluxes, CH4 producing and consuming microbial communities and sediment physico-chemical parameters in Z. noltei meadows and adjacent bare sediments across seven sites in Arcachon Bay, France. In situ CH4 fluxes were measured at low tide and microbial communities were characterised using targeted metagenomics of three functional genes (mcrA, mmoX, pmoA) and quantitative PCR. CH4 fluxes were higher in vegetated than bare sediments (24.4 +- 2.6 vs. 9.4 +- 0.7 micromol/m2/d). Mixed linear models and random forest analyses identified C accumulation rate and CO2 flux as the strongest positive descriptors of CH4 fluxes. Vegetated sediments hosted more diverse methanotrophs, while methanogens showed no habitat differences. Four genera (mcrA.Methanolobus, mmoX.Methylocella, pmoA.Methylococcus, Methyloglobulus) emerged as abundant, seagrass-associated, correlated with CH4 fluxes, and highlighted by models. Functional diversity, especially pmoA richness, was a stronger microbial descriptor of CH4 fluxes than gene abundance or a specific genus. Findings indicate Z. noltei meadows enhance C burial and CH4 emission, with methanotroph diversity potentially mitigating CH4 emissions. Our results provide the first integrated assessment of CH4 fluxes and their descriptors in Z. noltei meadows, highlighting the intertwined nature of C burial and CH4 emissions and the need to account for both in blue C climate assessments.