Modern crop varieties are typically cultivated in agriculturally well-managed soils far from the centers of origin of their wild relatives. How this habitat expansion impacted plant microbiome assembly is not well understood. Here, we investigated if the transition from a native to an agricultural soil affected rhizobacterial community assembly of wild and modern common bean (Phaseolus vulgaris) and if this led to a depletion of rhizobacterial diversity. The impact of the bean genotype on rhizobacterial assembly was more prominent in the agricultural soil than in the native soil. Although only 113 operational taxonomic units (OTUs) out of a total of 15,925 were shared by all eight bean accessions grown in native and agricultural soils, this core microbiome represented a large fraction (25.9%) of all sequence reads. More OTUs were exclusively found in the rhizosphere of common bean in the agricultural soil as compared to the native soil and in the rhizosphere of modern bean accessions as compared to wild accessions. Co-occurrence analyses further showed a reduction in complexity of the interactions in the bean rhizosphere microbiome in the agricultural soil as compared to the native soil. Collectively, these results suggest that habitat expansion of common bean from its native soil environment to an agricultural context had an unexpected overall positive effect on rhizobacterial diversity and led to a stronger bean genotype-dependent effect on rhizosphere microbiome assembly.