A growing body of evidence, particularly in humans and rodents, supports the existence of a complex network of interactions occurring between gastrointestinal (GI) helminth parasites and the gut commensal bacteria, with substantial effects on both host immunity and metabolic potential. However, little is known of the fundamental biology of such interactions in other animal species. Nonetheless, given the considerable economic losses associated with GI parasites, particularly in livestock and equines, as well as the global threat of emerging anthelmintic resistance, further explorations of the complexities of host-helminth-microbiota interactions in these species are needed. This study characterises, for the first time, the composition of the equine bacterial commensal flora associated with the presence, in faecal samples, of low (Clow) - and high (Chigh) numbers of eggs of an important group of equine GI parasites (i.e. the cyathostomins), prior to and following anthelmintic treatment. High-throughput sequencing of microbial 16S rRNA amplicons and associated bioinformatics and statistical analyses of sequence data revealed strong clustering according to faecal egg counts (FEC) (P = 0.003). A trend towards increased populations of Methanomicrobia (class) and Dehalobacterium (genus) was observed in Clow in comparison to Chigh. Anthelmintic treatment in Chigh was associated with a significant reduction of the bacterial phylum TM7 14 days post-ivermectin administration, as well as a transient expansion of Adlercreuzia spp. at 2 days post-treatment. This study provides a first insight into the discovery of the intimate mechanisms governing host-parasite-microbiota interactions in equids, and sets a basis for the development of novel, biology-based intervention strategies against equine GI helminths based on the manipulation of the commensal gut flora.