The domestication process not only reduced the allelic diversity of tomato genotypes but also affected the genetic traits associated to microbial recruitment, their composition, and their diversity in different compartments of the plant host. Additionally, this process included the transition from natural to agricultural soils, which differ in nutrient availability, physicochemical properties, and agricultural practices. Therefore, modern cultivars may fail to recruit microbial taxa beneficial to their wild relatives, potentially losing important ecological functions. In this study, we analyzed the phylogenetic relationship and the rhizosphere microbiota of four tomato genotypes, Solanum chilense (wild species), S. lycopersicum var. cerasiforme (Cherry tomato), and the S. lycopersicum landrace ‘Poncho Negro’ and the modern cultivar ‘Cal Ace’, grown in both natural and agricultural soils. Microbial communities were identified using 16S rRNA (bacteria) and ITS2 (fungi) amplicon sequencing, allowing cross-domain taxonomic characterization. While the soil type was the main driver of overall microbial diversity, the host genotype influenced the recruitment of specific microbial taxa, which exhibited different recruitment patterns according to the genetic diversification of Solanum genotypes and soil types. Additionally, co-occurrence network analysis identified two main clusters: first, taxa did not show any preferential associations to particular genotypes or soil types, while the second cluster revealed specific microbial patterns associated to fungal taxa in natural soil and bacterial taxa in agricultural soil. Finally, the functional analysis suggested the loss of specific functions through tomato domestication independently of soil type. These findings highlight the role of the plant genotype as a fine-tuning factor in microbiome assembly, with implications for breeding strategies aimed at restoring beneficial plant–microbe interactions.