Background Clostridioides difficile is an enteric pathogen historically known to cause hospital associated (HA)-infections in humans. A major risk factor for CDI in humans is antibiotic usage as it alters the gut microbiota and there is a loss of colonization resistance against C. difficile. In recent years there has been an increase in community associated (CA)-C. difficile infection that does not have the same risk factors as HA-CDI. Potential sources of CA-CDI have been proposed and include animals, food, water, and the environment, however these sources remain poorly investigated. Here, we define the prevalence of C. difficile strains found in different companion animals (canines, felines, and equines) to investigate a potential zoonotic link. C. difficile strains were identified by toxin gene profiling, fluorescent PCR ribotyping, and antimicrobial susceptibility testing. 16s rRNA gene sequencing was done on animal feces to investigate the relationship between the presence of C. difficile and the gut microbiota in different hosts. Results Here, we show that C. difficile was recovered from 20.9% of samples (42/201), which included 33 canines, 2 felines, and 7 equines. Over 69% (29/42) of the isolates were toxigenic and belonged to 14 different ribotypes, with overlap between HA- and CA-CDI cases in humans. The presence of C. difficile results in a shift in the fecal microbial community structure in both canines and equines. Commensal Clostridia C. hiranonis was negatively associated with C. difficile in canines. Further experimentation showed a clear antagonistic relationship between the two strains in vitro, suggesting that commensal Clostridia might play a role in colonization resistance against C. difficile in different hosts. Conclusions In this study we investigated a potentially important source of C. difficile transmission: the companion animal population. C. difficile carriage was common in dogs, cats, and horses. C. difficile isolates from companion animals included many of the same ribotypes known to cause HA- and CA-CDI in humans, and had similar antimicrobial resistance profiles as those isolated from human populations. These data contribute to our understanding of non-hospital exposure to C. difficile in the human population and suggest new avenues for reducing C. difficile prevalence in companion animals and, perhaps, thereby reducing CA-CDI in humans.