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Poplar plantations, widely used for the production of woody biomass, might be at high risk from the climate change-induced increase in the frequency of drought periods. Therefore, selecting improved genotypes, which are highly productive but with a high water use efficiency (WUE), is becoming a major target. The use of automated weighing systems in controlled environments facilitates the estimation of cumulated water loss and whole plant transpiration efficiency (TE). Differences in TE and leaf level intrinsic WUE as well as the contribution of underlying ecophysiological traits were determined in three contrasting P. nigra genotypes. Strong differences in TE among the selected genotypes were congruent with differences in leaf level intrinsic WUE. Our data show that a high total leaf area was overcompensated by a low per leaf area transpiration rate, leading to higher TE in highly productive genotypes originating from cool locations. Nocturnal water loss was relatively low but contributed to variations in TE among genotypes. In response to drought, leaf level WUE increased but not TE, suggesting that carbon losses due to whole plant respiration could offset the drought-induced increase in intrinsic WUE.