Many parasites with complex life-cycles alter the phenotype of their intermediate hosts in ways that seem to favor transmission to a final host. Although there is a large literature on host manipulation, how parasites alter the phenotype of their hosts remains poorly known. The bird acanthocephalan Polymorphus minutus is known to alter geotaxis in its amphipod host, Gammarus roeseli. Here we examine the potential roles of low oxygen availability and the excretion, by the parasite, of two products from its own anaerobic metabolism (lactate and succinate) in altered geotaxis. Under hypoxia, uninfected Gammarus roeseli showed negative geotaxis and lower metabolic rate, two traits also altered by infection with P. minutus, albeit with different intensities. The injection of a mixture of lactate and succinate in uninfected amphipods mimicked the parasite-induced reversion of geotaxis, without affecting the metabolic rate. In addition, both P. minutus-infected gammarids and uninfected ones conditioned to hypoxia for two days showed elevated levels of lactate in the brain, but not in the hemolymph. Overall, our results indicate that the pathways involved in anaerobic metabolism and hypoxia-signalling might be responsible for the changes in geotaxis and metabolic rate induced by P. minutus infection. Our study emphasizes the need to consider the tight and complex connections between physiological processes and behavioural adjustments, in particular at the brain level, in the understanding of parasitic manipulation, and more broadly of behavioural changes in infected hosts.