The perception of aphid infestation induces highly coordinated and sequential defensive reactions in plants at the cellular and molecular levels. The aim of the study was to explore kinetics of induced antioxidative defence responses in leaf cells of Pisum sativum L.cv. Cysterski upon infestation of the pea aphid Acyrthosiphon pisum at varying population sizes, including accumulation of flavonoids, changes of carbon metabolism, and expression of nuclear genes involved in sugar transport. Within the first 96 h, after A. pisum infestation, flavonoid accumulation and increased peroxidase activity were observed in leaves. The level of pisatin increased after 48 h of infestation and reached a maximum at 96 h. At this time point, a higher concentration of flavonols was observed in the infested tissue than in the control. Additionally, strong post-infestation accumulation of chalcone synthase (CHS) and isoflavone synthase (IFS) transcription products was also found. The levels of sucrose and fructose in 24-h leaves infested by 10, 20, and 30 aphids were significantly lower than in the control. Moreover, in leaves infested by 30 aphids, the reduced sucrose level observed up to 48 h was accompanied by a considerable increase in the expression level of the PsSUT1 gene encoding the sucrose transporter. In conclusion, A. pisum infestation on pea leads to stimulation of metabolic pathways associated with defence.