Stress responses are key for parasite survival and, consequently, also the evolutionary success of these organisms. Despite this importance, our understanding of the molecular pathways dealing with environmental stressors remains limited for parasitic animals. Here, we targeted the molecular pathways dealing with environmental stressors and comparatively investigated antioxidant, heat shock, osmoregulatory, and behaviour-related genes (foraging) in two parasitic flatworm lineages with contrasting species and ecological diversity, Cichlidogyrus and Kapentagyrus (Platyhelminthes: Monogenea), through whole-genome sequencing of 11 species. Using an in silico exon bait capture approach, we assembled the sequences of 48 stress-related genes and report the first foraging (for) gene orthologs in flatworms. We found duplications of heat shock- (hsp) and oxidative stress genes in Cichlidogyrus compared to Kapentagyrus. We also observed positive selection patterns in genes related to mitochondrial protein import (hsp) and behaviour (for) in species of Cichlidogyrus infecting East African cichlids—a host lineage under adaptive radiation—consistent with a potential adaptation linked to a co-radiation of parasites and hosts. Accordingly, this study potentially identifies the first molecular function linked to a flatworm radiation. Additionally, the absence of cytochrome P450, and kappa and sigma-class glutathione S-transferases in monogenean flatworms is reported, genes considered essential for metazoan life.