Although the vanilla spice is so well-known, there is an unexpected lack of knowledge on the domestication processes that have shaped its genetic resources. Within the main vanilla producing plant species, Vanilla planifolia, which has a long history of cultivation primarily through vegetative cuttings, unexpected high levels of genome-wide heterozygosity have been found in the global “Daphna” cultivar and in accessions cultivated in Mexico, its center of origin. These findings have pointed to a hybrid origin within the crop; however, the source and quantity of hybridization events remained unclear. This study aimed to disentangle these events by identifying parental candidate species and investigating the domestication processes underlying its hybrid origin. The less commonly cultivated species, V. pompona, was identified as a likely parental candidate and hypothesized to have hybridized with V. planifolia causing the high levels of genome-wide heterozygosity observed within cultivated individuals. Chromosomal structure and SNP distributions were compared between a V. planifolia “Daphna” cultivar, 15 V. planifolia accessions from Mexico, and one V. pompona accession to answer the questions: 1) do both haplotypes of the “Daphna” genome show signatures of hybridization with V. pompona?, 2) do the highly heterozygous Mexican V. planifolia accessions exhibit the same hybridization signatures as the “Daphna” genome?, and 3) do the latter accessions show signatures of one or multiple domestication events? Results provided evidence for multiple genomic origins within cultivated V. planifolia and revealed more variation than previously recognized. At least two distinct hybridization events were shown to have occurred: one showing signatures of introgressive hybridization between V. planifolia and V. pompona in the “Daphna” cultivar, and at least one more in Mexican cultivars. This parental origin, however, has yet to be identified. Additional research incorporating genomic data from other crop-wild relatives is necessary to further disentangle these events observed in Mexico. Findings from this study offer a clearer illustration of vanilla’s evolutionary history and genetic resources, highlight their importance for crop sustainability, and provide foundations for future research into the origin of this important spice.