The native holly leafminer Phytomyza glabricola is comprised of two host races on sister species of holly, Ilex glabra and I. coriacea. These native hosts are sympatric and may naturally hybridize in parts of their geographic range along the coast of the Eastern United States. Although adult leafminers associated with each host are morphologically indistinguishable, they display significant life history differences. P. glabricola develops in 2-4 weeks on I. glabra, whereas development takes 9-10 months on I. coriacea. P. glabricola from the two host plants show little mitochondrial DNA differentiation, but whole-genome AFLP frequency data show strong host plant based differences and a smaller differentiation among geographic locations. Herbarium specimens and personal observations suggest that morphological differentiation between I. glabra and I. coriacea varies among geographic location, likely caused by hybridization of these hollies. Such hybridization could weaken a barrier to gene exchange among leafminer host races and facilitate gene flow between host races across hosts, changing the dynamics of host race evolution and perhaps speciation in those locations where the hollies hybridize.