Drought intensity and frequency are increasing under global warming, with soil water availability now being a major factor limiting tree growth in circumboreal forests. Still, the adaptive capacity of trees in the face of future climatic regimes remains poorly documented. Using 1481 annually resolved tree‐ring series from 29‐yr‐old trees, we evaluated the drought sensitivity of 43 white spruce (Picea glauca (Moench) Voss) populations established in a common garden experiment. We show that genetic variation among populations in response to drought plays a significant role in growth resilience. Local genetic adaptation allowed populations from drier geographical origins to grow better, as indicated by higher resilience to extreme drought events, compared with populations from more humid geographical origins. The substantial genetic variation found for growth resilience highlights the possibility of selecting for drought resilience in boreal conifers. As a major research outcome, we showed that adaptive genetic variation in response to changing local conditions can shape drought vulnerability at the intraspecific level. Our findings have wide implications for forest ecosystem management and conservation.