Whole-genome duplication (polyploidy) and domestication are two of the most influential evolutionary drivers of plant diversification. However, little is known about their impact on microbiome structure and function broadly across phylogenetically distinct plant lineages. We conducted large-scale processing of publicly available amplicon datasets, co-occurrence network construction, and functional prediction profiling to determine whether polyploidy and domestication influenced microbiome communities across phylogenetically diverse plants. Our dataset consisted of 87 studies from around the globe that included 156 plant species with over 7000 sampled microbiomes. We found that polyploidy consistently structured phyllosphere but not rhizosphere microbiome properties, with effects largely conserved across prokaryotic and fungal communities. For phyllospheres, we found that domesticated polyploids had diversity levels similar to wild plants and that polyploids in general had significantly higher modularity, functional redundancy for abiotic stress mitigation, and enrichment of phosphorus-cycling enzymes. Taken together, our results collectively point to greater polyploid phyllosphere stability in fluctuating environments and enrichment in microbial taxa that assist in regulating plant growth during climate stress. In contrast, rhizosphere properties were driven primarily by geographic variables, suggesting rhizosphere responses are likely plant or environment-specific. These findings have broad implications for understanding how plant genome evolution shapes microbiome diversification.