The fast technological advances of molecular tools have enabled us to uncover a new dimension hidden within parasites and their hosts: their microbiomes. Increasingly, parasitologists characterise host microbiome changes in the face of parasitic infections, revealing the potential of these microscopic fast-evolving entities to influence host-parasite interactions. However, most of the changes in host microbiomes seem to depend on the host and parasite species in question. Furthermore, we should understand the relative role of parasitic infections as microbiome modulators when compared with other microbiome-impacting factors (e.g., host size, age, sex). Here, we characterised the microbiome of a single intermediate host species infected by two parasites belonging to different phyla: the acanthocephalan Plagiorhynchus allisonae and a dilepidid cestode, both infecting Transorchestia serrulata amphipods collected simultaneously from the same locality. We used the v4 hypervariable region of the 16S rRNA prokaryotic gene to identify the hemolymph bacterial community of uninfected, acanthocephalan-infected, and cestode-infected amphipods, as well as the bacteria in the amphipods’ immediate environment and in the parasites infecting them. Our results show that parasitic infections were more strongly associated with differences in host bacterial community richness than amphipod size, presence of amphipod eggs in female amphipods, and even parasite load. Amphipods infected by acanthocephalans had the most divergent bacterial community, with a marked decrease in alpha diversity compared with cestode-infected and uninfected hosts. In accordance with the species-specific nature of microbiome changes in parasitic infections, we found unique microbial taxa associating with hosts infected by each parasite species, as well as taxa only shared between a parasite species and their infected hosts. However, there were some bacterial taxa detected in all parasitised amphipods (regardless of the parasite species), but not in uninfected amphipods or the environment. We propose that shared bacteria associated with all hosts parasitised by distantly related helminths may be important either in helping host defences or parasites’ success, and could thus interact with host-parasite evolution.