Photoassimilates play crucial roles during plant-pathogen interactions, as colonizing pathogens rely on the supply of sugars from hosts. The competition for sugar acquisition at the plant-pathogen interface involves different strategies from both partners which are critical for the outcome of the interaction. Here, we dissect individual mechanisms of sugar uptake during the interaction of Arabidopsis thaliana with the necrotrophic fungus Botrytis cinerea using millicell culture insert, that enables molecular communication without physical contact. We demonstrate that B. cinerea is able to actively absorb glucose and fructose with equal capacities. Challenged Arabidopsis cells compete for extracellular monosaccharides through transcriptional reprogramming of host sugar transporter genes and activation of a complex sugar uptake system which displays differential specificity and affinity for hexoses. We provide evidence that the molecular dialogue between Arabidopsis cells and B. cinerea triggers major changes in host metabolism, including apoplastic sucrose degradation and consumption of carbohydrates and oxygen, suggesting an enhanced activity of the glycolysis and the cellular respiration. We conclude that beside a role in sugar deprivation of the pathogen by competing for sugar availability in the apoplast, the enhanced uptake of hexoses also contributes to sustain the increased activity of respiratory metabolism to fuel plant defences.