Drought stress causes crop yield losses worldwide. Sorghum is a C4 species tolerant to moderate drought stress, and its extensive natural variation for photosynthetic traits under water-limiting conditions can be exploited for developing cultivars with enhanced stress tolerance. The objective of this study was to discover genes/genomic regions that control the sorghum photosynthetic capacity under pre-anthesis water-limiting conditions. We performed a genome-wide association study for seven photosynthetic gas exchange and chlorophyll fluorescence traits during three periods of contrasting soil volumetric water content (VWC): control (30% VWC), drought (15% VWC), and recovery (30% VWC). Water stress was imposed with an automated irrigation system that generated a controlled dry-down period for all plants, to perform an unbiased genotypic comparison. A total of 60 genomic regions were associated with natural variation in one or more photosynthetic traits in a particular treatment or with derived variables. We identified 33 promising candidate genes with predicted functions related to stress signaling, oxidative stress protection, hormonal response to stress, and dehydration protection. Our results provide new knowledge about the natural variation and genetic control of sorghum photosynthetic response to drought with the ultimate goal of improving its adaptation and productivity under water stress scenarios.