Treatment with broad-spectrum antibiotics promotes the intestinal colonisation with vancomycin-resistant enterococci (VRE), where this intestinal colonisation often precedes the development of difficult-to-treat invasive VRE infections (e.g. bloodstream infections). Healthy gut microbiomes restrict VRE growth in the intestine, however broad-spectrum antibiotics significantly disrupt the gut microbiome and make the host susceptible to VRE intestinal colonisation. Therefore, understanding how antibiotics disrupt the gut microbiome will allow us to develop new treatments to prevent or treat VRE intestinal colonisation, which will prevent the subsequent development of invasive VRE infections. We showed that antibiotics (that promote VRE intestinal colonisation) killed gut commensals, enriched for a wide range of nutrients, and depleted a wide range of microbial metabolites. We found that a mixture of short chain fatty acids (that were depleted with antibiotics treatment) provided complete or near complete inhibition of VRE growth. We also showed that monosaccharides, disaccharides, and amino acids (that were enriched with antibiotic treatment) acted as carbon or nitrogen sources to promote VRE growth. Finally, we showed that vancomycin-resistant Enterococcus faecium and Enterococcus faecalis occupied overlapping but distinct nutrient-defined intestinal niches where each pathogen achieved high growth when cultured with each other and when cultured with other multidrug-resistant pathogens (carbapenem-resistant Enterobacteriaceae). In summary, we showed that VRE can grow in antibiotic-treated intestines by utilising specific enriched nutrients while in the presence of reduced concentrations of inhibitory microbial metabolites.