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Exploitation of natural resources is a driver of human infectious disease emergence. The emergence of animal reservoirs of Guinea worm Dracunculus medinensis, particularly in domestic dogs Canis familiaris, has become the major impediment to global eradication of this human disease. 93% of all Guinea worms detected worldwide in 2020 were in dogs in Chad. Novel, non-classical pathways for transmission of Guinea worm in dogs, involving consumption of fish, have been hypothesized to support the maintenance of this animal reservoir. We quantified and analyzed variation in Guinea worm emergence in dogs in Chad, across three climatic seasons, in multiple villages and districts. We applied forensic stable isotope analyses to quantify dietary variation within and among dogs and GPS tracking to characterize their spatial ecology. At the end of the hot-dry season and beginning of the wet season, when fishing by people is most intensive, Guinea worm emergence rates in dogs were highest, dogs ate most fish, and fish consumption was most closely associated with disease. Consumption of fish by dogs enables a non-classical transmission pathway for Guinea worm in Chad. Seasonal fisheries and the facilitation of dogs eating fish are likely contributing to disease persistence and to this key impediment to human disease eradication. Interrelated natural resource use, climatic variation, companion animal ecology, and human health highlight the indispensability of One Health approaches to the challenges of eradicating Guinea worm and other zoonotic diseases.