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In the late 1990s, the San Miguel Island fox (Urocyon littoralis littoralis) faced near-extinction. Fourteen of the 15 remaining foxes were placed into an island-based captive breeding program used to repopulate the island. Although the fox population in San Miguel reached pre-decline numbers by 2010, a second decline started around 2014, coincidental with a newly observed acanthocephalan parasite. To identify this introduced acanthocephalan species and determine the pathologic consequences of its infection on the health of foxes, we used an extensive record of island fox necropsies and associated parasite collections. In addition, we used detailed fox capture-recapture data to investigate population health and demographic trends of foxes before and after parasite emergence. We identify the parasite as Pachysentis canicola, a common acanthocephalan in mainland foxes in North America. The parasite was detected in 69% of the necropsied foxes from San Miguel Island and was not found in any of the other five Channel Island fox subspecies. Health impacts attributed to the acanthocephalan parasite, including erosive and ulcerative enteritis, transmural necrosis, and inflammation, were described in 47% of the foxes infected with the acanthocephalan. Despite infection with various other helminth parasite species, body condition remained good and the mortality rate low in San Miguel Island foxes until the arrival of the acanthocephalan. Body condition improved after 2018, perhaps due to increases in rainfall following a drought, but remained 27% lower than the pre-acanthocephalan period, which suggests that environmental conditions and parasitism jointly drive fox population dynamics., (Copyright © 2024 Australian Society for Parasitology. All rights reserved.)