Recently diverged populations often exhibit incomplete reproductive isolation, with a low level of gene flow continuing between populations. Previous studies have shown that, even under a low level of gene flow, genetic divergence between populations can proceed at the loci governing local adaptation and reproductive isolation but not at other neutral loci. A leaf-mining moth, Acrocercops transecta, consists of Juglans- and Lyonia-associated host races. The two host races differ in host preferences of ovipositing females and in larval adaptation to host plants but mate readily in the laboratory, producing fertile hybrids. The Juglans and Lyonia races are often sympatric in the wild, implying that gene introgression could occur in nature between the two host races. We tested this hypothesis by combining phylogenetic analyses with coalescent simulations, focusing on mitochondrial genes (COI and ND5) and the nuclear Tpi, Per and Ldh genes located on the Z-chromosome. The mitochondrial genes clearly distinguished the Lyonia race from the Juglnas race, whereas the Tpi, Per and Ldh genealogies did not reflect the two host races. Coalescent simulations indicated gene flow at the three Z-linked genes in both directions, whereas there was no introgression in the mitochondrial genes. The lack of introgression in mitochondrial genes suggests that female host preference is the primary force leading to the bifurcation of maternally inherited loci. Thus, the results show that a low level of gene flow coupled with the inflexible female host preference differentiates histories of divergence between maternally and biparentally inherited genes in this host race system.