Several northern freshwater fishes have gone through rapid adaptive radiation after the last glacial period, resulting in new species or intraspecific morphs with distinct life histories. Parasite infections can promote adaptive radiations and spatiotemporal differences in patterns of infections can potentially reveal incipient or ongoing speciation processes. We investigated intraspecific differentiation in a freshwater gadoid fish, burbot (Lota lota), by exploring differences in parasite infections between two potential life-history morphs in Lake Konnevesi, Central-Finland, one reproducing species characteristically in shallow littoral waters in February and the other possibly in deep profundal zone roughly a month later. By conducting a sampling campaign on reproducing fish over two consecutive years, we found significant differences in infections between the fish captured from littoral and profundal sites. More specifically, larval trematode and cestode infections were consistently less abundant in profundal fish, tracking long-term exposure differences in shallow waters. In contrast, trophically transmitted metazoan infections in the fish gut, reflecting shorter-term differences in feeding, showed higher variation between sampling years rather than depths. We also found suggestive evidence of higher trematode-inflicted tissue damage per parasite in the profundal fish, implying lower tolerance to the infection. These results offer further evidence that burbot captured from littoral and profundal sites represent differentiated life-history morphs. We propose that ecological and evolutionary differentiation within burbot populations across its circumpolar distribution may be more widespread than previously acknowledged.