Parasites are increasingly being recognised as important players affecting individuals, populations, communities, and even ecosystems. Some parasites change their host’s behaviour to aid transmission to the next host in their life cycle. Parasite-induced behaviour modification may both drive and be driven by changes in host energy metabolism. Here, we examined the gregarious estuarine fish species, the California killifish (Fundulus parvipinnis) and its brain-infecting, behaviour-manipulating trematode parasite (Euhaplorchis californiensis). Killifish were reared in shoals from hatching in either a control (uninfected) or twice-weekly infection (infected) treatment for 12 months. Standard metabolic rate (SMR), maximum metabolic rate (MMR), and acute metabolic response to infectious propagules (MRacute) were then measured using respirometry chambers that allowed these social fish to smell and see their shoal-mates to prevent isolation stress. Brain, gill, and white muscle samples were extracted to assess the way infection influences citrate synthase (CS) and lactate dehydrogenase (LDH) enzymatic activities as indicators of aerobic and anaerobic metabolism, respectively. While SMR and MMR were unaffected by infection status, both uninfected and infected fish exhibited spikes in MRacute. Intriguingly, infected fish mounted a stronger response to exposure than naïve (control) hosts, implying a learned ‘fear’ response to parasite exposure. Measures of enzyme activity suggested that only the brain (the site of the infection) was impacted by the parasites, with infected individuals exhibiting lower LDH activity than uninfected fish. Given the importance of lactate in brain function, these results could suggest a mechanism for parasiteinduced behavioural modification.