Sphagnum wetlands show relatively low methane (CH₄) emissions, primarily due to efficient CH₄ oxidation by methanotrophs inhabiting the hyaline cells of Sphagnum. However, the impact of Sphagnum-derived antimicrobial metabolites on soil CH₄ emissions is not clear. Here, we conducted two comparative experiments to elucidate how sphagnum acid, which accounts for >40% of Sphagnum-derived phenolic metabolites, regulates soil CH₄ emissions in order to evaluate its potential to mitigate CH₄ emissions (extracellularly) relative to Sphagnum planting (intracellularly). In Experiment 1, 24 soil columns from six Sphagnum-dominated wetlands were incubated for 30 days to measure CH₄ fluxes with and without a Sphagnum layer in order to establish a benchmark for the CH₄ mitigation capacity of living Sphagnum. Live Sphagnum reduced CH₄ emissions by ∼70%, with reductions in fluxes positively correlated with Sphagnum biomass. In Experiment 2, 21 surface soils from seven non-Sphagnum wetlands were incubated for 105 days with the addition of sphagnum acid in comparison with ferrihydrite and glucose to assess the isolated effects of these exogenous substrates/materials on CH₄ emissions. Microbial communities were analyzed using amplicon sequencing and quantitative real-time polymerase chain reaction. Notably, sphagnum acid markedly reduced methanotroph abundance, indirectly promoting soil CH₄ emissions. The decline in methanotroph was primarily driven by the inhibitory effects of water-soluble phenols in soils, outweighing the potential stimulatory effects of reactive iron oxides that were abundant in Sphagnum wetlands. In contrast, hydrogenotrophic methanogens dominating in our soils, particularly Methanobacterium, were not affected by sphagnum acid amendment. Collectively, this study highlights that wetland CH₄ mitigation efforts should prioritize conserving and restoring Sphagnum vegetation over the application of exogenous phenolic metabolites.