Microorganisms play key roles in influencing the primary productivity, carbon sequestration and greenhouse gas budgets of mangrove ecosystems. In the mangrove sediments, specialized bacteria and archaea compete for energy and resources to inhabit optimal ecological niches and can produce or consume methane – a potent greenhouse gas – in the process. The production, accumulation and cycling of methane in mangrove sediments have gained growing attention, yet uncertainties remain regarding the exact functional and spatial distributions of microorganisms driving these processes, as well as the mechanisms responsible for lateral and vertical transport of methane. In the study presented here, we use amplicon sequencing to assess communities of bacteria and archaea related to the methane cycle in a pristine mangrove forest. We show that atypical niches for methanogen communities exist in the upper tidal salt marsh zone where vegetation is sparse. Surprisingly, the highest proportion of methanogenic archaea in the studied ecosystem continuum was detected at the hypersaline salt marsh end of the continuum despite a relatively high redox potential. Methane concentrations were highest at the lowest depth within the mangrove forest and coincided with both the highest methane sediment fluxes and high methanotroph abundance at the sediment surface. We suggest that methane from deeper sediments is outgassed via crab burrows and pneumatophores bypassing oxidation. The spatial data from this study highlights the importance of investigating methane dynamics across elevation and vegetation gradients in estuarine ecosystems and underpins the vital role of pristine coastal vegetation zones in the face of a changing climate.