Heterosis or hybrid vigor is common in hybrid poplars, and to investigate its occurrence and physiological basis we compared narrowleaf cottonwoods, Populus angustifolia James, prairie cottonwoods, Populus deltoides Bartr. ex Marsh, and their native intersectional hybrids, P. × acuminata Rydb., from Alberta, Canada. Clonal replicates from 10 separate trees from each taxon were raised in growth chambers at different temperatures (T). Growth was similarly vigorous across the taxa at 20 and 24 °C, and morphological and physiological traits of the hybrids were generally intermediate between the parental species, or similar to the larger parent, demonstrating additive inheritance or dominance, respectively. Growth declined at 18 and 15 °C particularly in the parental species, and consequently hybrid vigor was displayed for root and especially leaf growth. Stomatal distributions and chlorophyll indices were intermediate in the hybrids and unaffected by T. Foliar nitrogen (N), net assimilation (Asat), stomatal conductance (gs) and transpiration (E) per unit of leaf area were lower in the hybrids, but the hybrids generally had larger leaf areas. Water-use efficiencies (Asat/gs) were similar across the taxa and reduced with warming, while nitrogen-use efficiencies (Asat/N) increased. δ13C was correlated with leaf mass per area, which varied across the taxa. Photosynthesis (Asat) was correlated with chlorophyll content index, N and/or gs in P. deltoides and the hybrids, but not in P. angustifolia, indicating different physiological limitations. We conclude that heterosis in P. × acuminata results from the compound benefits from multiple dominant traits, and superior growth particularly at suboptimal conditions. This indicates phenotypic stability or environmental adaptability, whereby heterozygosity provides metabolic diversity that allows hybrids to thrive across a broader environmental range.