While dynamic regulation of photosynthesis in fluctuating light is increasingly recognized as an important driver of carbon uptake, acclimation to realistic patterns of light fluctuations is still largely unexplored. We subjected Arabidopsis thaliana (L.) plants to light fluctuations with distinct amplitudes and average irradiance. Using gas-exchange and thermal imaging, we examined how light fluctuations affected leaf structure, photosynthetic capacity, and water relations. We found a wider amplitude of fluctuations produced a stronger acclimation response. Large reductions of leaf mass per area under fluctuating light framed our interpretation of changes in pigment content and photosynthetic capacity, in that photosynthetic investment increased markedly on a mass basis, but only a little on an area basis. Moreover, leaf transpiration rose sharply, being nearly four times under fluctuating light. Our findings indicate that leaves growing under fluctuating light, although thinner, maintained their photosynthetic capacity; suggesting their photosynthesis may be more cost-efficient than those under steady light, but overall may incur increased maintenance costs. This is especially relevant for plant performance globally, because naturally fluctuating light created conflicting acclimation cues for photosynthesis and transpiration that may hinder progress towards ensuring food security under climate-related extremes of water stress.