Conventional agricultural activity reduces the uptake of the potent greenhouse gas methane by agricultural soils. However, the recently observed improved methane uptake capacity of agricultural soils after compost application is promising but needs mechanistic understanding. In this study, the methane uptake potential and microbiomes involved in methane cycling were assessed in green compost and household-compost with and without pre-digestion. In bottle incubations of different composts with both high and near-atmospheric methane concentrations (∼10.000 & ∼10 ppmv, respectively), green compost showed the highest potential methane uptake rates (up to 305.19 ± 94.43 nmol h−1 g dw compost−1 and 25.19 ± 6.75 pmol h−1 g dw compost−1, respectively). 16S, pmoA and mcrA amplicon sequencing revealed that its methanotrophic and methanogenic communities were dominated by type Ib methanotrophs, and more specifically by Methylocaldum szegediense and other Methylocaldum species, and Methanosarcina species, respectively. Ordination analyses showed that the abundance of type Ib methanotrophic bacteria was the main steering factor of the intrinsic methane uptake rates of composts, whilst the ammonium content was the main limiting factor, being most apparent in household composts. These results emphasize the potential of compost to contribute to methane mitigation, providing added value to compost as a product for industrial, commercial, governmental and public interests relevant to waste management. Compost could serve as a vector for the introduction of active methanotrophic bacteria in agricultural soils, potentially improving the methane uptake potential of agricultural soils and contributing to global methane mitigation, which should be the focus of future research.