The nature and strength of interactions entertained among helminths and their host gut microbiota remain largely unexplored. Using 40 naturally infected Welsh ponies, we tracked the gut microbiota-cyathostomin temporal dynamics during parasite community removal and reassembly, and the associated host immune response. Infected ponies harboured 14 species of cyathostomins, overwhelmed by the abundance of Cylicocyclus nassatus. Parasite carriers exhibited gut environment modifications, higher Shannon entropy and orderly rearrangements of prokaryotic assemblages, with protective Clostridia species contributing to the successional nemabiome-microbiota crosstalk. Yet, the gut ecosystem was remarkably stable, and the host systemic response defined enrichment for B-cell activation and IgA production without corresponding changes in parasite burdens. Therefore, Clostridia microbial protection likely reduced fluctuating dynamics between the microbiota-parasite-host triad and favoured parasite tolerance. The system stability was disrupted by pyrantel treatment and parasite removal, with dire early consequences on the gut environment, microbiota diversity, and cytokine networks while highlighting the detrimental effect of cyathostomin burdens on Enterococcus spp. Both ecological communities were highly resilient to disturbance and recovered their pre-treatment compositions but for Cylicostephanus longibursatus in the parasite community. However, gut microbiotas failed to restore their original stability and shifted towards an interacting unstable state, with transient coexistence between Clostridia and core bacterial taxa, e.g. Fibrobacter and Prevotella, evoking their crucial role as stabilising forces for this new equilibrium. These observations highlight how anthelmintic treatment alters the gut microbiota stability and open new perspectives for adding nutritional intervention to current parasite management strategies in the field.