Endolithic cyanobacteria are ubiquitous colonisers of organic and inorganic carbonate substrata that frequently attack the shells of mussels, eroding the shell to extract carbon, often with population infestation rates of >80%. This reduces host physiological condition and ultimately leads to shell collapse and mortality, compromising the services provided by these important ecosystem engineers. While the ecological implications of this and similar interactions have been examined, our understanding of the underlying mechanisms driving the physiological responses of infested hosts remains limited. Using field and laboratory experiments, we assessed the energetic costs of cyanobacterial infestation to the intertidal brown mussel (Perna perna). In the field we found that growth (measured as both increase in shell length and rate of biomineralization) and reproductive potential of clean mussels are greater than those of infested individuals. To explore the mechanisms behind these effects, we compared the energy allocation of parasite-free and infested mussels using the scope for growth (SFG) framework. This revealed a lower SFG in parasitized mussels attributed to an energetic imbalance caused by increased standard metabolic rates, without compensation through increased feeding or reduced excretion of ammonia. Separate laboratory assays showed no differences in calcium uptake rates, indicating that infested mussels do not compensate for shell erosion through increased mineralization. This suggests that the increased maintenance costs detected reflect repair of the organic component of the inner nacreous layer of the shell, an energetically more demanding process than mineralization. Thus, parasite-inflicted damage reduces SFG directly through the need for increased basal metabolic rate to drive shell repair without compensatory increases in energy intake. This study provides a first perspective of the physiological mechanisms underlying this parasite-host interaction, a critical step towards a comprehensive understanding of the ecological processes driving dynamics of this intertidal ecosystem engineer.