Polyploidization and transposon elements contribute to shape plant genome diversity and secondary metabolic variation in some edible crops. However, the specific contribution of these variations to the chemo-diversity of Lamiaceae, particularly in economic shrubs, is still poorly documented. The rich essential oils (EOs) of Lavandula plants are distinguished by monoterpenoids among the main EO-producing species, L. angustifolia (LA), L. × intermedia (LX) and L. latifolia (LL). Herein, the first allele-aware chromosome-level genome was assembled using a lavandin cultivar 'Super' and its hybrid origin was verified by two complete subgenomes (LX-LA and LX-LL). Genome-wide phylogenetics confirmed that LL, like LA, underwent two lineage-specific WGDs after the γ triplication event, and their speciation occurred after the last WGD. Chloroplast phylogenetic analysis indicated LA was the maternal source of 'Super', which produced premium EO (higher linalyl/lavandulyl acetate and lower 1,8-cineole and camphor) close to LA. Gene expression, especially the monoterpenoid biosynthetic genes, showed bias to LX-LA alleles. Asymmetric transposon insertions in two decoupling 'Super' subgenomes were responsible for speciation and monoterpenoid divergence of the progenitors. Both hybrid and parental evolutionary analysis revealed that LTR (long terminal repeat) retrotransposon associated with AAT gene loss cause no linalyl/lavandulyl acetate production in LL, and multi-BDH copies retained by tandem duplication and DNA transposon resulted in higher camphor accumulation of LL. Advances in allelic variations of monoterpenoids have the potential to revolutionize future lavandin breeding and EO production.