Sea otters are an endangered keystone species in coastal ecosystems for which relatively little is known about their indigenous microbiota. The microbiota of animals is relevant to conservation because it reveals and integrates diet, nutritional status, pathogen exposure, and other elements of host health and disease. To characterize the indigenous bacterial community structure of southern sea otters (Enhydra lutris nereis), we used 16S rRNA gene amplicon sequencing to study 145 gingival (oral), 121 rectal, and 79 adjacent seawater samples from 148 individual wild sea otters living off the coast of central California, USA. Comparisons of wild and captive sea otter rectal samples suggested that captivity does not significantly alter community structure of the distal gut microbiota. Bacterial communities in the sea otter gut were distinct from those of freshwater otters, such as the North American river otter. Based on unsupervised machine learning analysis, sea otter gingival community structure displayed three different profiles. To understand better the functional potential of the sea otter gut microbiome, we performed shotgun metagenomic sequencing on 12 fecal samples. These data unexpectedly revealed that the majority of DNA in these samples appeared to be derived from prey (at least 63% in one case) rather than from indigenous bacteria or host cells as with most other mammals. We speculate that a reduced bacterial biomass in the sea otter gut reflects a short intestinal tract, rapid transit time, and particular strategy for foraging and energy harvest. This study establishes a baseline for understanding the structure of the microbiota of healthy sea otters, which may assist in future health assessments and conservation management of sea otter populations and of sick or vulnerable animals.