Globally, parasites are sensitive toward environmental changes, and, in some cases, they are even more sensitive than their hosts. However, there is limited knowledge on the physiological responses of parasites and their effects on their hosts in relation to environmental degradation. In this study, metallothioneins (MTs) were isolated and compared between the ectoparasite Lamproglena clariae and its host fish Clarias gariepinus. Differences in the levels of MTs in the parasite and host were compared to physicochemical water quality variables and metals to determine if MT expression was linked with changes in water quality. Clarias gariepinus individuals were sampled from 2 sites of differing water quality along the Vaal River using gill nets and assessed for L. clariae. Gill, muscle, and liver tissue of the host and L. clariae were collected and stored in liquid nitrogen for analysis of MT. Water and sediment samples were collected for metal analysis by inductively coupled plasma–optical emission spectrometry and inductively coupled plasma–mass spectrometry. Nutrient levels and water hardness in water samples were assessed using spectrophotometry. MTs were quantified using spectrophotometry and size exclusion chromatography in the host and parasite, respectively. Infections by L. clariae differed between sites, with higher parasite intensity at the unpolluted Vaal Dam site. Concentrations of MT in host tissues and L. clariae were significantly higher at the polluted site, below the Vaal River Barrage, compared to the Vaal Dam site. Parasite MT concentrations were significantly lower compared to concentrations in the liver and gill tissue of C. gariepinus individuals. In conclusion, differences in the concentrations of MT and infection biology of L. clariae reflected the state of the environment and support the usefulness of this parasite and other Lamproglena spp. as bioindicators.