Climate change can strongly alter soil microbial functioning via plant–microbe interactions, often with important consequences for ecosystem carbon and nutrient cycling. Given the high degree of intraspecific trait variability in plants, it has been hypothesized that genetic shifts within plant species yield a large potential to control the response of plant–microbe interactions to climate change. Here we examined if sea-level rise and plant genotype interact to affect soil microbial communities in an experimental coastal wetland system, using two known genotypes of the dominant salt-marsh grass Elymus athericus characterized by differences in their sensitivity to flooding stress – i.e., a tolerant genotype from low-marsh environments and an intolerant genotype from high-marsh environments. Plants were exposed to a large range of flooding frequencies in a factorial mesocosm experiment, and soil microbial activity parameters (exo-enzyme activity and litter breakdown) and microbial community structure were assessed. Plant genotype mediated the effect of flooding on soil microbial community structure and determined the presence of flooding effects on exo-enzyme activities and belowground litter breakdown. Larger variability in microbial community structure, enzyme activities, and litter breakdown in soils planted with the intolerant plant genotype supported our general hypothesis that effects of climate change on soil microbial activity and community structure can depend on plant intraspecific genetic variation. In conclusion, our data suggest that adaptive genetic variation in plants could suppress or facilitate the effects of sea-level rise on soil microbial communities. If this finding applies more generally to coastal wetlands, it yields important implications for our understanding of ecosystem–climate feedbacks in the coastal zone.