Avian haemosporidian parasites are globally widespread with a broad repertoire of hosts. When infected, the host can either reduce the parasite burden (resistance) and/or limit the severity of parasitaemia (tolerance). Oxidative stress is known to play a pivotal role in the host’s resistance and tolerance as well as its detrimental endpoints. The rationale behind this paradox lies in the dual role of reactive oxygen species (ROS): they can have both beneficial and detrimental effects for the host, while being largely harmful to the parasite. Thus, it is in the parasite’s interest to maintain a reduced environment within the host’s cell, whereas the host needs a fine-tuned balance between generating ROS to eliminate the parasites and maintaining sufficient antioxidant levels to protect its own tissues. This dynamic is what we refer to as the host-parasite oxidative arms-race. In this study, Eurasian siskins (Spinus spinus) were experimentally infected with Plasmodium ashfordi to investigate how the fundamental antioxidant system – the glutathione redox-system – responds to infection over time compared to control birds. By combining physiological measures and gene expression data of key glutathione related genes from both the parasite and the host at different time points, we provide evidence of this oxidative arms race. The gene expression data show that the parasite actively maintains reduced intracellular environment and eliminates ROS through high expression of superoxide dismutase (SOD), glutathione reductase (GR), and glutathione synthetase. In contrast, the host upregulates glutathione S-transferases (GSTs) and glutathione peroxidases (GPX), which reduce the physiologically active levels of the key antioxidant, glutathione. Although, the parasite seems to win the race in terms of the oxidative state of the cell, the marked decrease in parasitaemia from day 21 (45%) to 31 (15%) suggests that the host’s strategy by lowering the physiological glutathione levels is sufficient to defeat the parasite.