It is increasingly recognized that different genetic variants of hosts can uniquely shape their microbiomes. Invasive species often evolve in their introduced ranges, but little is known about the potential for their microbial associations to change during invasion as a result. We asked whether host genotype (G), microbial environment (E), or their interaction (G × E) affected the composition and diversity of host-associated microbiomes in Centaurea solstitialis (yellow starthistle), a Eurasian plant that is known to have evolved novel genotypes and phenotypes and to have altered microbial interactions, in its severe invasion of CA, USA. We conducted an experiment in which native and invading plant genotypes were inoculated with native and invaded range soil microbial communities. We used amplicon sequencing to characterize rhizosphere bacteria in both the experiment and the field soils from which they were derived. We found that native and invading plant genotypes accumulated different microbial associations at the family level in each soil community, often counter to differences in family abundance between soil communities. Root associations with potentially beneficial Streptomycetaceae were particularly interesting, as these were more abundant in the invaded range field soil and accumulated on invading genotypes. We also found that bacterial diversity is higher in invaded soils, but that invading genotypes accumulated a lower diversity of bacteria and unique microbial composition in experimental inoculations, relative to native genotypes. Thus variation in microbial associations of invaders was driven by the interaction of plant G and microbial E, and rhizosphere microbial communities appear to change in composition in response to host evolution during invasion.