Abatus agassizii is an irregular sea urchin species that inhabits shallow waters of South Georgia and South Shetlands Islands. As a deposit-feeder, A. agassizii nutrition relies on the ingestion of the surrounding sediment in which it lives barely burrowed. Despite the low complexity of its feeding habit, it harbors a long and twice-looped digestive tract suggesting that it may host a complex bacterial community. Here, we characterized the gut microbiota of specimens from two A. agassizii populations at the south of the King George Island in the West Antarctic Peninsula. Using a metabarcoding approach targeting the 16S rRNA gene, we characterized the Abatus microbiota composition and putative functional capacity, evaluating its differentiation among the gut content and the gut tissue in comparison with the external sediment. Additionally, we aimed to define a core gut microbiota between A. agassizii populations to identify potential keystone bacterial taxa. Our results show that the diversity and the composition of the microbiota, at both genetic and predicted functional levels, were mostly driven by the sample type, and to a lesser extent by the population location. Specific bacterial taxa, belonging mostly to Planctomycetacia and Spirochaetia, were differently enriched in the gut content and the gut tissue, respectively. Predictive functional profiles revealed higher abundance of specific pathways, as the sulfur cycle in the gut content and the amino acid metabolism, in the gut tissue. Further, the definition of a core microbiota allowed to obtain evidence of specific localization of bacterial taxa and the identification of potential keystone taxa assigned to the Desulfobacula and Spirochaeta genera as potentially host selected. The ecological relevance of these keystone taxa in the host metabolism is discussed.