Background and Aims <p>The plant-associated microbiomes, which are shaped by plant domestication and environmental selections, further affect host various phenotypic traits and are essential for improving plant productivity. Although host genetic factors are known to build the assembly of microbial communities at the plant-soil interface, the effects of host evolution history or genome evolution on rhizosphere microbiome remains unclear.</p> Methods <p>Upon the nine years of planting history of field experiment, coupled with multi-omics analysis, we investigated the consequences of complex plant evolutionary history in rhizosphere microbiome.</p> Results <p>Our results showed that wheat rhizosphere microbiomes were co-shaped by both plant genotype and evolutionary history. Significant asynchrony was observed in microbial responses to domestication, hexaploidization, and cultivation. Metagenomic analysis revealed that domestication and hexaploidization preferentially enriched microbial taxa encoding genetic modules for carbohydrate and nitrogen compound utilization. Subsequent cultivation practices further shaped the rhizosphere microbiome, driving functional capacity toward enhanced carbohydrate metabolism. The representation of 29 high-quality, non-redundant metagenome-assembled genomes (MAGs) from bacteria revealed stable facultative chemotrophic lifestyles with capacities for carbon, nitrogen, iron, and sulfur cycling.</p> Conclusion <p>Our study demonstrates that host plant evolution drives asynchronous shifts in core bacterial and fungal communities while significantly altering microbial functional genes, particularly those involved in carbon and nitrogen cycling, yet maintains the conservation of key metabolic pathways across evolutionary stages. These findings enhance our understanding of the dynamics of rhizosphere functional adaptation throughout plant evolution and could guide rewilding strategies for crop productivity in sustainable agriculture.</p>