Enterobacter cloacae is a clinically important Gram-negative member of the Enterobacteriaceae, which has increasingly been recognized as a major pathogen in nosocomial infections. Despite this, knowledge about the population structure and the distribution of virulence factors and antibiotic-resistance determinants of this species is scarce. In this study, we analysed a systematic collection of multidrug-resistant E. cloacae isolated between 2001 and 2011 from bloodstream infections across hospitals in the UK and Ireland. We found that the population is characterized by the presence of multiple clones formed at widely different time periods in the past. The clones exhibit a high degree of geographical heterogeneity, which indicates extensive dissemination of these E. cloacae clones across the UK and Ireland. These findings suggest that a diverse, community-based, commensal population underlies multidrug-resistant E. cloacae infections within hospitals.