Aphids can affect the growth or architecture of their host-trees, but rarely challenge their survival. Nonetheless, the woolly poplar aphid, Phloeomyzus passerinii, can kill healthy, mature poplars during outbreaks. Trees fail to open their buds and flush their leaves in the spring following a severe infestation. This insect develops on poplar trunks, where it induces galls which accumulate amino acids and deplete starch content in the bark tissues. Here, we hypothesized that an infestation may then reduce non-structural carbohydrates (NSC) and non-structural nitrogen compounds (NSNC) contents in the bark, and that the reduction would be positively correlated with the infestation duration. This would in turn compromise the spring reactivation of trees. Consequently we also hypothesized that the bark contents of NSC and NSNC could be positively correlated with the amount of branches exhibiting bud break in spring, and the subsequent radial growth. The bark contents of NSC and NSNC were quantified in autumn for poplars exhibiting different levels of infestation and located in two distant stands. In one stand, NSC and NSNC contents in the bark were also quantified in the following spring and the damage level in the crowns were evaluated. In both stands, the infestation dramatically reduced the NSC and NSNC contents in autumn, especially starch and protein contents. While the drop in protein content was not related to infestation duration, the starch content gradually decreased when infestation duration increased. The infestation effect on starch content was still detectible in spring, after reserves had likely been mobilized for the spring reactivation. Starch content in autumn and spring was strongly positively correlated with crown health and radial increment. These results suggest that poplars infested by P. passerinii may die from carbon reserves deficiency, which would be an unprecedented situation for tree-aphid and tree-gall inducing insects interactions. Further experiments monitoring seasonal dynamics of NSC and NSNC reserves in different organs of infested trees should be conducted to validate this hypothesis. The results also suggest that the starch content in the bark of infested trees, in autumn, might be used as a predictor of tree decay by managers.