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In soybean, limiting whole-plant transpiration rate (TR) response to increasing vapor pressure deficit (VPD) has been associated with the slow-wilting phenotype and with water-conservation enabling higher yields under terminal drought. Despite the promise of this trait, it is still unknown whether it has a genetic basis in soybean, a challenge limiting the prospects of breeding climate-resilient varieties. Here we present the results of a first attempt at a high-throughput phenotyping of TR and stomatal conductance response curves to increasing VPD conducted on a soybean mapping population consisting of 140 recombinant inbred lines (RIL). This effort was conducted over two consecutive years, using a controlled-environment, gravimetric phenotyping platform which enabled characterizing 900 plants for these responses, yielding regression parameters (R2 from 0.92 to 0.99) that were used for genetic mapping. Several quantitative trait loci (QTL) were identified for these parameters on chromosomes (Ch) 4, 6 and 10, including a VPD-conditional QTL on Ch 4 and a constitutive QTL controlling all parameters on Ch 6. This study demonstrated for the first time that canopy water use in response to rising VPD has a genetic basis in soybean, opening novel avenues for identifying alleles enabling water conservation under current and future climate scenarios.