Rapid climate warming in the Arctic results in multifaceted disruption of biodiversity, faunal structure, and ecosystem health. Hypotheses have linked range expansion and emergence of parasites and diseases to accelerating warming globally but empirical studies demonstrating causality are rare. Using historical data and recent surveys as baselines, we explored climatological drivers for Arctic warming as determinants of range expansion for two temperature-dependent lungworms, Umingmakstrongylus pallikuukensis and Varestrongylus eleguneniensis, of muskoxen (Ovibos moschatus) and caribou (Rangifer tarandus), in the Canadian Arctic Archipelago from 1980 through 2017. Our field data shows a substantial northward shift of the northern edge of the range for both parasites and increased abundance across the expanded ranges during the last decade. Mechanistic models parameterized with parasites' thermal requirements demonstrated that geographical colonization tracked spatial expansion of permissive environments, with a temporal lag. Subtle differences in life histories, thermal requirements of closely related parasites, climate oscillations and shifting thermal balances across environments influence faunal assembly and biodiversity. Our findings support that persistence of host-parasite assemblages reflects capacities of parasites to utilize host and environmental resources in an ecological arena of fluctuating opportunity (alternating trends in exploration and exploitation) driving shifting boundaries for distribution across spatial and temporal scales.