While group formation provides antipredatory defences, increases foraging efficiency and mating opportunities, it can be counterintuitive by promoting disease transmission amongst social hosts. Upon introduction of a pathogen, uninfected individuals often modify their social preferences to reduce infection risk. Infected hosts also exhibit behavioural changes, for example, removing themselves from a group to prevent an epidemic. Conversely, here we show how Trinidadian guppies infected with a directly transmitted ectoparasite, Gyrodactylus turnbulli, significantly increase their contact rates with uninfected conspecifics. As uninfected fish never perform this behaviour, this is suggestive of a parasite-mediated behavioural response of infected hosts, presumably to offload their parasites. In the early stages of infection, however, such behavioural modifications are ineffective in alleviating parasite burdens. Additionally, we show that fish exposed to G. turnbulli infections for a second time, spent less time associating than those exposed to parasites for the first time. We speculate that individuals build and retain an infection cue repertoire, enabling them to rapidly recognize and avoid infectious conspecifics. This study highlights the importance of considering host behavioural modifications when investigating disease transmission dynamics.