Abstract Understanding the impact of the oak shothole leafminer Japanagromyza viridula (Coquillett) (Diptera: Agromyzidae) on oaks is important because oaks provide invaluable ecological services in forests and urban settings. In 2019 and 2020, shothole leafminers caused high levels of damage to oak trees in several states in the mid-Atlantic region. The objectives of this study were to compare oak shothole leafminer damage on the genus Quercus L. (Fagales: Fagaceae) including northern red oak (Quercus rubra L), chestnut oak (Q. montana Willd.), white oak (Q. alba L), scarlet oaks (Quercus coccinea Münchh.), and to fill critical knowledge gaps of oak shothole leafminer biology. Leaf area reduction, percent damaged leaves, foliage transparency, and crown dieback were calculated to compare damage experienced by the different oak species. Emergence and Malaise traps were used to assess adult population sizes. Chestnut oak was consistently the oak species with the least leaf area reduction and foliage transparency. The injuries on chestnut oak leaves were primarily small and uniform holes (“shotholes”) due to this leafminer. In contrast, northern red oak and scarlet oaks showed high susceptibility. Damaged leaves of these species frequently were deformed or incomplete, and the shotholes varied in size, resulting in greater leaf area reduction. Experiments showed that the conspicuous shothole damage caused by this leafminer is related to puncturing by the female flies into leaves of young buds. In conclusion, oak shothole leafminer is a native cryptic pest and outbreaks are visually apparent only when emergence coincides with oak bud and early leaf development.