Cultivation and naturalization of plants beyond their natural range can bring previously geographically isolated taxa together, thereby increasing the opportunity for hybridization and inter-specific gene flow, the outcomes of which are not predictable. These anthropogenic events therefore allow us to study how hybridization and inter-specific gene flow affect genetic and phenotypic diversity. Here, we explore the phenotypic and genomic effects of increased inter-specific gene flow following the re-introduction of the cultivated Mentha spicata (spearmint) into the ranges of the native mints M. longifolia and M. suaveolens. Using morphological analyses, we show that the cultivated M. spicata has altered trichome characters, which is likely a product of human imposed selection for a more palatable plant or a byproduct of selection on essential oil production. Using whole genome sequencing, we then show that there is extensive genetic admixture between the morphologically defined mint taxa that to some extent is mediated by the cultivated M. spicata. This has, at least partially, resulted in a breakdown of the species barriers. However, despite this breakdown, we find that genetic variants associated with the cultivated trichome morphology continue to segregate in cultivated, naturalized, and wild populations and we identify three genes that may function in the production of the characteristic aromatic oils of mints. Although hybridization can increase species richness by forming new hybrid taxa, we here show that unless reproductive barriers are strong it can also merge species into population/coalescent complexes over evolutionary time.