Microbes in marine sediments constitute up to five-sixths of the planet’s total biomass, but their diversity is little explored, especially for those forming associations with unicellular protists. Heterotrophic ciliates are among the most dominant and diversified marine benthic protists and comprise hotspot niches of bacterial colonization. To date, studies using culture-independent single-cell approaches to explore microbiomes of marine benthic ciliates in nature are almost absent, even for the most ubiquitous species. Here, we characterize the major bacterial groups associated with a representative marine benthic ciliate,Geleiasp. YT, collected directly from the coastal zone of Yantai, China. PacBio sequencing of the nearly full-length 16Sr RNA genes was performed on single cells ofGeleia. Fluorescence in situ hybridization (FISH) analysis with genus-specific probes was further applied to locate the dominant bacterial groups. We identified aVariovorax-like bacterium as the major epibiotic symbiont residing in the kineties of the ciliate host. We provide evidence of a nucleus-associated bacterium related to the human pathogenMycoplasma, which appeared prevalently in the local populations ofGeleiasp. YT for 4 months. The most abundant bacterial taxa associated withGeleiasp. YT likely represent its core microbiome, hinting at the important roles of the ciliate-bacteria consortium in the marine benthos. Overall, this work has contributed to the knowledge of the diversity of life in the enigmatic marine benthic ciliate and its symbioses.