ABSTRACT Wetland restoration on peat islands previously drained for agriculture has potential to reverse land subsidence and sequester atmospheric carbon dioxide as peat accretes. However, the emission of methane could potentially offset the greenhouse gas benefits of captured carbon. As microbial communities play a key role in governing wetland greenhouse gas fluxes, we are interested in how microbial community composition and functions are associated with wetland hydrology, biogeochemistry, and methane emission, which is critical to modeling the microbial component in wetland methane fluxes and to managing restoration projects for maximal carbon sequestration. Here, we couple sequence-based methods with biogeochemical and greenhouse gas measurements to interrogate microbial communities from a pilot-scale restored wetland in the Sacramento-San Joaquin Delta of California, revealing considerable spatial heterogeneity even within this relatively small site. A number of microbial populations and functions showed strong correlations with electron acceptor availability and methane production; some also showed a preference for association with plant roots. Marker gene phylogenies revealed a diversity of major methane-producing and -consuming populations and suggested novel diversity within methanotrophs. Methanogenic archaea were observed in all samples, as were nitrate-, sulfate-, and metal-reducing bacteria, indicating that no single terminal electron acceptor was preferred despite differences in energetic favorability and suggesting spatial microheterogeneity and microniches. Notably, methanogens were negatively correlated with nitrate-, sulfate-, and metal-reducing bacteria and were most abundant at sampling sites with high peat accretion and low electron acceptor availability, where methane production was highest. IMPORTANCE Wetlands are the largest nonanthropogenic source of atmospheric methane but also a key global carbon reservoir. Characterizing belowground microbial communities that mediate carbon cycling in wetlands is critical to accurately predicting their responses to changes in land management and climate. Here, we studied a restored wetland and revealed substantial spatial heterogeneity in biogeochemistry, methane production, and microbial communities, largely associated with the wetland hydraulic design. We observed patterns in microbial community composition and functions correlated with biogeochemistry and methane production, including diverse microorganisms involved in methane production and consumption. We found that methanogenesis gene abundance is inversely correlated with genes from pathways exploiting other electron acceptors, yet the ubiquitous presence of genes from all these pathways suggests that diverse electron acceptors contribute to the energetic balance of the ecosystem. These investigations represent an important step toward effective management of wetlands to reduce methane flux to the atmosphere and enhance belowground carbon storage.