Bloom-forming marine gelatinous zooplankton, including the pelagic tunicate Dolioletta gegenbauri, occur circumglobally and have the potential to significantly influence the structure of pelagic marine food webs and biogeochemical cycling through interactions with microbial communities. Using targeted metabarcoding (16S rRNA genes recovering Bacteria/Archaea) and qPCR approaches associated with laboratory-based feeding experiments, we characterized patterns in doliolid gut microbiomes and microbial communities associated with doliolid fecal pellets and the surrounding seawater. The characterization of starved doliolids provides the first description of the doliolid gut microbiome. At the highest taxonomic levels, doliolid-associated bacterial communities are characteristic of marine bacterioplankton communities around the globe and were dominated by representatives of six major bacterial groups including Gammaproteobacteria, Alphaproteobacteria, Cyanobacteria, Planctomycetes, Bacteroidia and, Phycisphaerae. Comparison between sample types, however, revealed distinct patterns in diversity and biomass supporting the hypothesis that through their presence and trophic activity, doliolids influence the structure of pelagic food webs and biogeochemical cycling in subtropical continental shelf systems where doliolid blooms are common. Bacteria associated with starved doliolids (representative of the resident doliolid gut microbiome) possessed distinct communities, supporting the hypothesis that doliolids possess a unique but low diversity, low biomass microbiome optimized to support a detrital trophic mode. Among potential core microbiome taxa, the genera Pseudoalteromomas and Shimia were the most abundant, similar to patterns observed in other marine invertebrates. Exploratory bioinformatic analyses of predicted functional genes suggest that doliolids, via their interactions with bacterial communities, may affect important biogeochemical processes including nitrogen, sulfur, and organic matter cycling.