The diffusible toxin ColIb produced by Salmonella enterica serovar Typhimurium SL1344 is a potent inhibitor of Escherichia coli growth. To identify and parameterize metabolic cross-feeding in states of competition, we established defined communities in which E. coli was the only species able to access a sole carbon source, lactose. Although ColIb was predicted to undermine cross-feeding by killing the lactose-converting E. coli, S. enterica populations thrived in co-culture. We discovered that ColIb caused the release of active β-galactosidase from E. coli cells, which induced galactose uptake by S. enterica. Although iron limitation stimulates ColIb production and makes E. coli more sensitive to the toxin, ColIb killing in iron-limited conditions did not enhance iron acquisition or siderophore scavenging by S. enterica. Also unexpected was the rapid rate at which resistance to ColIb evolved in E. coli through spontaneous mutation of the ColIb receptor gene cirA or horizontal acquisition of the S. enterica colicin immunity gene imm. Mathematical modelling effectively predicted the growth kinetics of E. coli and S. enterica populations, revealing a tractable system in which ColIb can shrink a competitor population while simultaneously amplifying the metabolic contributions of the suppressed population.