Summary Photosynthesis in woody tissues ( P wt ) is less sensitive to water shortage than in leaves, hence, P wt might be a crucial carbon source to alleviate drought stress. To evaluate the impact of P wt on tree drought tolerance, woody tissues of 4‐m‐tall drought‐stressed Populus tremula trees were subjected to a light‐exclusion treatment across the entire plant to inhibit P wt . Xylem water potential ( Ψ xylem ), sap flow ( ), leaf net photosynthesis ( P n,l ), stem diameter variations (Δ D ), in vivo acoustic emissions in stems (AEs) and nonstructural carbohydrate concentrations ([NSC]) were monitored to comprehensively assess water and carbon relations at whole‐tree level. Under well‐watered conditions, P wt kept Ψ xylem at a higher level, lowered and had no effect on [NSC]. Under drought, Ψ xylem , and P n,l in light‐excluded trees rapidly decreased in concert with reductions in branch xylem starch concentration. Moreover, sub‐daily patterns of Δ D , and AEs were strongly related, suggesting that in vivo AEs may inform not only about embolism events, but also about capacitive release and replenishment of stem water pools. Results highlight the importance of P wt in maintaining xylem hydraulic integrity under drought conditions and in sustaining NSC pools to potentially limit increases in xylem tension.