The gastro-intestinal (GI) microbiota of abalone contains a highly complex bacterial assemblage playing an essential role in the overall health of these gastropods. The gut bacterial communities characterized so far reveal considerable interspecific variability, likely resulting from bacterial interactions and constrained by the ecology of their host species; however, they remain poorly investigated. Additionally, the extent to which structural changes in the microbiota entail functional shifts in metabolic pathways of bacterial communities remains unexplored. In order to address these questions, we characterized the gut microbiota of the northeast Pacific blue ( Haliotis fulgens or HF) and yellow ( Haliotis corrugata or HC) abalone by 16S rRNA 454 pyrosequencing to shed light on: ( i) their gut microbiota structure; ( ii) how bacteria may interact among them; and ( iii) predicted shifts in bacterial metabolic functions associated with the observed structural changes. Our findings revealed that Mycoplasma dominated the GI microbiome in both species. However, the structure of the bacterial communities differed significantly in spite of considerable intra-specific variation. This resulted from differences of the species with most reads in each GI metagenome, suggesting host-specific adaptation of bacterial lineages to these sympatric abalone. We hypothesize that the presence of exclusive OTUs in each microbiota may relate to host-specific differences in competitive pressure. Significant differences in bacterial diversity were found for the explored metabolic pathways between species despite their functional overlap. A more diverse array of bacteria contributed to each function in HC, whereas a single or much fewer OTUs were generally observed in HF. The structural and functional analyses allowed us to describe a deep taxonomic and functional split between the microbiota of HF and HC abalone.