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Background We assessed metrics of the metazoan parasite infracommunities of the dusky flounder ( Syacium papillosum ) as indicators of aquatic environmental health of the Yucatan Shelf (YS) prior to oil extraction. We sampled the dusky flounder and its parasites along the YS, mostly during the 2015 north wind season (November–April). Our aims were: (i) to determine whether the parasite infracommunity metrics of S. papillosum exhibit significant differences among YS subregions; (ii) to determine whether the probability of the occurrence of its parasite species and individuals were affected by environmental variables, nutrients, heavy metals and hydrocarbons at the seascape level; and (iii) to determine whether there were statistical differences between the parasite infracommunity metrics of S. papillosum from YS and those of Syacium gunteri from the Campeche Sound. Multivariate statistical analyses and generalised additive models (GAMs) were used to examine the potential statistical associations between the contaminants, environmental variables and parasite community metrics, and the maximum entropy algorithm (MaxEnt) was used to characterise the habitat’s suitability for the parasite’s probability of occurrence. Results We recovered 48 metazoan parasite species from 127 S. papillosum , with larval cestodes and digeneans being the most numerically-dominant. Multivariate analyses showed significant differences in parasite infracommunity metrics among Western YS, Mid YS and Caribbean subregions, with the latter being the richest in species but not in individuals. The GAM and MaxEnt results indicated a negative effect of top predators (e.g. sharks and rays) removal on parasite metrics. The parasite infracommunities of S. papillosum were twice as rich in the number of species and individuals as those reported for S. gunteri from the Campeche Sound. Conclusions The significant differences among subregions in parasite metrics were apparently due to the interruption of the Yucatan current during the north wind season. The fishing of top predators in combination with an influx of nutrients and hydrocarbons in low concentrations coincides with an increase in larval cestodes and digeneans in S. papillosum . The dusky flounder inhabits a region (YS) with a larger number of metazoan parasite species compared with those available for S. gunteri in the Campeche Sound, suggesting better environmental conditions for transmission in the YS. Electronic supplementary material The online version of this article (10.1186/s13071-019-3524-6) contains supplementary material, which is available to authorized users.