Landfills generate outsized environmental footprints due to microbial degradation of organic matter in municipal solid waste, which produces the potent greenhouse gas methane. With global solid waste production predicted to increase substantially in the next few decades, there is a pressing need to better understand the temporal dynamics of biogeochemical processes that control methane cycling in landfills. Here, we use metagenomic approaches to characterize microbial methane cycling in waste that was landfilled over 39 years. Our analyses indicate that newer waste supports more diverse communities with similar composition compared to older waste, which contains lower diversity and more varied communities. Older waste contains primarily autotrophic organisms with versatile redox metabolisms, whereas newer waste is dominated by anaerobic fermenters. Methane-producing microbes are more abundant, diverse, and metabolically versatile in new waste compared to old waste. Our findings indicate that predictive models for methane emission in landfills overlook methane oxidation in the absence of oxygen, as well as certain microbial lineages that can potentially contribute to methane sinks in diverse habitats.