Simple Summary Enteropathogenic Escherichia coli (EPEC) from cattle receive little attention, although some belong to the most notorious O serotypes of attaching/effacing Shigatoxigenic Escherichia coli (AE-STEC) responsible for the uremic and hemolytic syndrome in humans, such as O26. Nevertheless, the O serotypes and virulotypes of the large majority of bovine EPEC remain unidentified. This study aimed to identify five non-classical O serotypes (O123/186, O156, O177, O182, and O183) by a polymerase chain reaction (PCR) among three collections of bovine EPEC from young diarrheic calves, healthy cattle at slaughterhouses, and healthy calves in dairy farms. The virulotypes and sequence types (STs) obtained after the whole genome sequencing of several O156, O177, and O182 bovine EPEC were closely related or identical to the virulotypes and STs of ten bovine and the human AE-STEC of the same O:H serotype. This study allows us to identify more EPEC O serotypes from cattle and to speculate on their evolution. Enteropathogenic Escherichia coli (EPEC) produce attaching/effacing (AE) lesions and cause non-bloody diarrhea in mammals. A minority of bovine EPEC belong to one of the ten classical serotypes of human and bovine AE-STEC. The purpose of this study was to identify five non-classical O serotypes (O123/186, O156, O177, O182, and O183) among bovine EPEC and to characterize their virulence repertoires by whole genome sequencing. Around 40% of the 307 EPEC from 307 diarrheic calves, 368 EPEC from 47 healthy cattle, and 131 EPEC from 36 healthy calves in dairy farms were analyzed. Serotype O177 was the most frequent among EPEC from diarrheic and healthy calves, while the O156 was the most frequent in healthy cattle. The genomic analysis identified different H serotypes, MLSTypes, and/or eae gene subtypes among the O156 and O177 EPEC, while the O182 was homogeneous. The virulence gene profiles of bovine EPEC were closely related to each other and to the profiles of ten bovine and human AE-STEC. These results emphasize ...