Poplars are important fast-growing, water-spending biomass tree crops. Here, we targeted the wax biosynthesis pathway of Populus × canescens by overexpressing jojoba (Simmondsia chinensis) wax ester synthase (ScWS) for the production of lipids. We found that ScWS overexpression caused accumulation of lipid droplets in leaf cells but did not increase wax load on the leaf surface. However, the stomata had a high fraction of closed or semi-closed guard cells with aberrant lipid accumulation. This phenotype was accompanied by suppression of OCCLUDED STOMATAL PORE 1 (OSP1) and decreased stomatal conductance in the ScWS-expressing poplars. During short- and long-term drought scenarios under greenhouse and outdoor conditions, the ScWS lines had increased water use efficiencies, leading to a water-saving phenotype and delays in drought stress. In the ScWS poplars, photosynthesis was reduced under high, but not under low light intensities. Biomass production of ScWS lines was unaffected in short-term experiments but dropped below that of wild-type poplars at the end of two field seasons, indicating a long-term growth trade-off. Our results open new opportunities for the production of lipids in more water-efficient poplars.