Factors that drive continental-scale variation in root microbiota and plant adaptation are poorly understood. We monitored root-associated microbial communities in Arabidopsis thaliana and co-occurring grasses at 17 European sites across 3 years. We observed strong geographic structuring of the soil biome, but not of the root microbiota. A few phylogenetically diverse and geographically widespread bacteria consistently colonized plant roots. Among-site and across-year similarity in microbial community composition was stronger for the bacterial root microbiota than for filamentous eukaryotes. In a reciprocal transplant between two A. thaliana populations in Sweden and Italy, we uncoupled soil from location effects and tested their contributions to root microbiota variation and plant adaptation. Community differentiation in plant roots was explained primarily by location for filamentous eukaryotes and by soil origin for bacteria, whereas host genotype effects were marginal. Strong local adaptation between the two A. thaliana populations was observed, with differences in soil properties and microbes of little importance for the observed magnitude of adaptive differentiation. Our results suggest that, across large spatial scales, climate is more important than soil conditions for plant adaptation and variation in root-associated filamentous eukaryotic communities, whereas soil properties are primary drivers of bacterial community differentiation in roots.