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Despite the importance of plant–plant interactions on plant community dynamics and crop yield, our understanding of the adaptive genetics underlying these interactions is still limited and deserves to be investigated in the context of complex and diffuse interactions occurring in plant assemblages. Here, based on 145 natural populations of Arabidopsis thaliana located in south-west of France and characterized for plant communities, we conducted a Genome– Environment Association analysis to finely map adaptive genomic regions of A. thaliana associated with plant community descriptors. To control for correlated abiotic environment effects, we also characterized the populations for a set of biologically meaningful climate and soil variables. A non-negligible fraction of top single nucleotide polymorphisms was associated with both plant community descriptors and abiotic variables, highlighting the importance of considering the actual abiotic drivers of plant communities to disentangle genetic variants for biotic adaptation from genetic variants for abiotic adaptation. The adaptive loci associated with species abundance were highly dependent on the identity of the neighboring species suggesting a high degree of biotic specialization of A. thaliana to members of its plant interaction network. Moreover, the identification of adaptive loci associated with alpha-diversity and composition of plant communities supports the ability of A. thaliana to interact simultaneously with multiple plant neighbors, which in turn can help to understand the role of community-wide selection. Altogether, our study highlights that dissecting the genetic basis underlying plant–plant interactions at a regional scale while controlling for abiotic confounding factors can help understanding the adaptive mechanisms modulating natural plant assemblages.