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The myometrium, composed of the inner circular muscle (CM) and outer longitudinal muscle (LM), is crucial in establishing and maintaining early pregnancy. However, the molecular mechanisms involved are not well understood. In this study, we identified the transcriptomic features of the CM and LM collected from the mesometrial (M) and anti-mesometrial (AM) sides of the pig uterus on day 18 of pregnancy during the placentation initiation phase. Some genes in the cellular zinc ion level regulatory pathways (MT-1A , MT-1D , MT-2B , SLC30A2 , and SLC39A2) were spatially and highly enriched in uterine CM at the mesometrial side. In addition, the histone modification profiles of H3K27ac and H3K4me3 in uterine CM and LM collected from the mesometrial side were characterized. Genomic regions associated with the expression of genes regulating the cellular zinc ion level were detected. Moreover, six highly linked variants in the H3K27ac-enriched region of the pig SLC30A2 gene were identified and found to be significantly associated with the total number born at the second parity (P < 0.05). In conclusion, the genes in the pathways of cellular zinc homeostasis and their regulatory elements identified have implications for pig reproduction trait improvement and warrant further investigations. • The myometrium includes the circular muscle (CM) and longitudinal muscle (LM) layers. • Genes in the cellular zinc homeostasis pathway were highly enriched in pig uterine CM. • Genomic regions related to gene expression that regulate zinc ion levels were detected. • Six variants in the H3K27ac-enriched region upstream of the SLC30A2 gene were associated with litter size in pigs. [ABSTRACT FROM AUTHOR]