The myxozoan Henneguya ictaluri is the cause of proliferative gill disease (PGD) in US farm-raised channel (Ictalurus punctatus) and channel (I. punctatus) × blue (Ictalurus furcatus) catfish hybrids. Colloquially known as “hamburger gill”, PGD is arguably the most important parasitic disease of commercial catfish aquaculture in the southeastern United States. Research indicates arrested sporogenesis occurs in hybrid catfish, yet PGD persists in hybrid catfish production systems. These reports suggest other myxozoans besides H. ictaluri may be associated with PGD. Further, it is hypothesized host susceptibility drives myxozoan diversity in catfish pond aquaculture systems. This work investigated the influence of catfish host on myxozoan community composition within 1) naturally infected gill tissues from clinical PGD cases and 2) pond water associated with channel and hybrid catfish monoculture. For three years, DNA extracted from gills of diagnostic case submissions with clinical PGD, as well as water from experimental ponds dedicated to either channel or hybrid catfish monoculture, were analyzed by metagenomic sequencing to compare myxozoan community composition and diversity between catfish species and assess year-over-year trends. Myxozoan community composition significantly differed between channel and hybrid systems in both gill and pond water datasets for all three years examined. Channel catfish gills had greater relative abundance of H. ictaluri in 2017 and 2019 and unclassified taxa in 2018 compared to hybrid catfish. H. ictaluri was present in all channel and hybrid catfish PGD cases, although in nearly half of these clinical PGD cases H. ictaluri was not the most abundant myxozoan. In the pond experiment, H. ictaluri relative abundance was significantly greater in channel catfish ponds in years 2 & 3. In hybrid catfish ponds, H. ictaluri never exceeded 20% average relative abundance. Both datasets revealed hybrid catfish monoculture can selectively suppresses H. ictaluri proliferation. This work suggests crop rotation strategies could mitigate disease by preventing H. ictaluri from reaching levels associated with catastrophic losses. Further, detection of numerous known and unclassified myxozoan sequences provides evidence PGD may involve mixed species infections. Furthermore, the scores of unclassified myxozoan sequences present in gill and pond water samples indicates the number of described species vastly underestimates the true myxozoan diversity present within the varied microcosms associated with catfish aquaculture. Future work will investigate the potential contribution of other myxozoans to gill pathology in PGD outbreaks in channel and hybrid catfish production systems.