In northern Japan, Q. mongolica var. crispula (Qc) is common in inland habitats, and Q. dentata (Qd) occurs in coastal habitats. At the northern distributional limit of Qd, Q. × angustilepidota (Qa), a hybrid taxon between Qc and Qd, occurs in coastal habitats. These taxa were transplanted to inland and coastal common gardens (sites). Genotypes at 27495 loci, phenotypes of eight traits of leaves and shoots, and 30-year-old tree size were measured for 224 individuals in both sites. Genotypic variation revealed a hybrid zone between Qc and Qd, including both northern-edge Qd admixed with Qc and coastal Qa backcrossed to Qc. Phenotypes of Qa trees were intermediate between those of Qc and Qd trees. Size of Qa and Qd trees was smaller than that of Qc trees in the inland site but was larger in the coastal site, suggesting adaptation of Qa and Qd to coastal environment. Local ancestry was estimated from phased genotypes of admixed trees using 47 Qc and 25 Qd reference trees, indicating heterogeneous ancestry along chromosomes. Association mapping of genotypes and admixture mapping of ancestry suggested that some loci potentially associated with four traits were related to stress response and were located at introgressed genomic regions.