To investigate if Clostridium (Clostridioides) difficile infection (CDI), traditionally thought of as hospital‐acquired, can be genomically linked to hospital or community environmental sources, and to define possible importation routes from the community to the hospital.

In 2019, C. difficile was isolated from 89/300 (29.7%) floor and 96/300 (32.0%) shoe sole samples at a tertiary hospital in Western Australia. Non‐toxigenic C. difficile ribotype (RT) 010 predominated among floor (96.6%) and shoe sole (73.2%) isolates, while toxigenic RT 014/020 was most prevalent among contemporaneous clinical cases (33.0%) at the hospital. Whole‐genome sequencing and high‐resolution core genome single nucleotide polymorphism (cgSNP) analysis on C. difficile strains from hospital and community sources showed no clinical C. difficile RT 014/020 strains were genetically related, and evidence of frequent long‐distance, multi‐directional spread between humans, animals and the environment. In addition, cgSNP analysis of environmental RT 010 strains suggested transportation of C. difficile via shoe soles.

While C. difficile RT 014/020 appears to spread via routes outside the healthcare system, RT 010 displayed a pattern of possible importation from the community into the hospital.

These findings suggest developing community‐based infection prevention and control strategies could significantly lower rates of CDI in the hospital setting.