Oregano is an important economic plant which has valuable medicinal and aromatic properties. Oregano essential oil, containing carvacrol and thymol, is a preferred material to replace antibiotics in feed additives. Glandular secretory trichome (GST) density has positively correlated with the production of these compounds. Here, two haplotype-resolved genomes were assembled and annotated which contained 15 chromosomes with the total length of 606.75 and 612.74 Mb, respectively. Oregano had experienced two whole-genome duplications corresponding to the divergence ~5.120/4.564 and ~66.857/69.923 Mya, respectively. Many transcription factors and genes were found related to GSTs formation mechanism such as R2R3-MYB- and HD-ZIP IV-encoding genes. 2,669,410 SNPs, 569,093 InDels, 14,839 DUPs, 110 INVs, 3,976 TRANSs, and 1,426 CNVs were detected among two haplotype-resolved genomes. Two high density genetic linkage maps consisted of 15 LGs and spanned 2,279.28 and 2,322.83 cM, respectively. GADS, GABS, and GTS of F2 segregating populations showed obvious superparental dominance. One/one, one/one, and two/four QTLs for GADS, GABS, and GTS were independently mapped on two genetic maps, respectively. Five candidate genes showed extreme difference in two bulked segregant pools. Our study not only provides significant insight into the GSTs formation mechnism, but also will facilitate molecular breeding in oregano.