The rhizosphere microbiome is important for plant growth and health, contributing to nutrient acquisition and (a)biotic stress tolerance. Rhizosphere microbiome composition is shaped in part by the plant genotype, but the underlying genetic basis is largely unknown. Going back to the roots, we investigated how plant domestication affected rhizosphere microbiome assembly of common bean (Phaseolus vulgaris), a key food crop worldwide. DArT genotyping and plant phenotyping showed substantial genetic diversity and root architectural differences between ancestral and modern bean accessions grown in Colombian field soil. Bean genotypes affected rhizosphere microbiome composition, with Bacteroidetes and Verrucomicrobia enriched on roots of ancestral beans and Actinobacteria more prevalent on modern beans. Genome-wide association mapping pinpointed single nucleotide polymorphisms (SNPs) in the bean genome associated with the abundance of specific rhizobacterial families. SNPs identified in chromosomes 3 and 4 were positioned at loci associated with signaling, lignin biosynthesis and pathogen resistance.