Perennially frozen soils that are common in higher-latitude ecosystems are predicted to release large amounts of methane as permafrost thaws, exacerbating ongoing climate warming. However, methane emissions from soils represent the outcome of two competing microbial processes, methane production via methanogenesis and consumption via methane oxidation. How this balance mitigates the impacts of permafrost thaw on methane emissions remains largely undetermined as the rate and spatial variation of methane emissions are not currently well constrained. We measured vegetation cover, active layer depth, and methane fluxes from 392 locations across 92 gradually or abruptly thawing sites in interior Alaska, USA. We performed 16S rRNA gene and shotgun metagenomic sequencing on a subset of 92 surface soils from these sites. Most sites exhibited low or negative methane emissions, while a subset of poorly drained, abruptly thawing sites had elevated methane fluxes, which corresponded to sites with high relative abundances of patchily distributed hydrogenotrophic Methanobacteriaceae methanogens. Methanotrophs were detected in all samples and were dominated by novel, putative methanotrophs from the Methylacidiphilales (Verrucomicrobiota) order and the Mycobacterium (Actinomycetota) and Rhodopila (Pseudomonadota) genera, which together had greater relative abundances than canonical methanotrophs. This result was supported by both 16S rRNA gene sequencing, analysis of pmoA and mmoX sequences from shotgun metagenomes, and gene content analysis of metagenome-assembled genomes. The ubiquity and high abundances of these understudied putative methanotrophs potentially explain why so many of our surveyed sites had negative methane fluxes and may represent a globally important sink for methane emissions from thawing permafrost.