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Abstract Within the North American boreal forest, a widespread outbreak of the epidermal leaf miner Phyllocnistis populiella has damaged quaking aspen (Populus tremuloides) for nearly 20 years. In a series of experiments, we tested the effects of feeding damage by P. populiella on leaf water relations and gas exchange. Relative to insecticide-treated trees, the leaves of naturally-mined trees had lower photosynthesis, stomatal conductance to water vapor, transpiration, water use efficiency, predawn water potential, and water content, as well as more enriched foliar δ13C. The magnitude of the difference between naturally-mined and insecticide-treated trees did not change significantly throughout the growing season, suggesting the effect is not caused by accumulation of incidental damage to mined portions of the epidermis over time. The contributions of mining-related stomatal malfunction and cuticular transpiration to these overall effects were investigated by restricting mining damage to stomatous abaxial and astomatous adaxial leaf surfaces. Mining of the abaxial epidermis decreased photosynthesis and enriched leaf δ13C, while increasing leaf water potential and water content relative to unmined leaves; effects consistent with stomatal closure due to disfunction of mined guard cells. Mining of the adaxial epidermis also reduced photosynthesis but had different effects on water relations, reducing midday leaf water potential and water content relative to unmined leaves, and did not affect δ13C. In the laboratory, extent of mining damage to the adaxial surface was positively related to the rate of water loss by leaves treated to prevent water loss through stomata. We conclude that overall, despite water savings due to closure of mined stomata, natural levels of damage by P. populiella negatively impact water relations due to increased cuticular permeability to water vapor across the mined portions of the epidermis. Leaf mining by P. populiella could exacerbate the negative effects of climate warming and water deficit in interior Alaska.