Understanding how genetic differences among soil microorganisms regulate spatial patterns in litter decay remains a persistent challenge in ecology. Despite fine root litter accounting for ~50% of total litter production in forest ecosystems, far less is known about the microbial decay of fine roots relative to aboveground litter. Here, we evaluated whether fine root decay occurred more rapidly where fungal communities have a greater genetic potential for litter decay. Additionally, we tested if linkages between decay and fungal genes can be adequately captured by delineating saprotrophic and ectomycorrhizal fungal functional groups based on whether they have genes encoding certain ligninolytic class II peroxidase enzymes, which oxidize lignin and polyphenolic compounds. To address these ideas, we used a litterbag study paired with fungal DNA barcoding to characterize fine root decay rates and fungal community composition at the landscape scale in northern temperate forests, and we estimated the genetic potential of fungal communities for litter decay using publicly available genomes. Fine root decay occurred more rapidly where fungal communities had a greater genetic potential for decay, especially of cellulose and hemicellulose. Fine root decay was positively correlated with ligninolytic saprotrophic fungi and negatively correlated with ECM fungi with ligninolytic peroxidases, likely because these saprotrophic and ectomycorrhizal functional groups had the highest and lowest genetic potentials for plant cell wall degradation, respectively. These fungal variables overwhelmed direct environmental controls, suggesting fungal community composition and genetic variation are primary controls over fine root decay in temperate forests at regional scales.