Abstract Stable social bonds in group-living animals can provide greater access to food. A striking example is that female vampire bats often regurgitate blood to socially bonded kin and nonkin that failed in their nightly hunt. Food-sharing relationships form via preferred associations and social grooming within roosts. However, it remains unclear whether these cooperative relationships extend beyond the roost. To evaluate if long-term cooperative relationships in vampire bats play a role in foraging, we tested if foraging encounters measured by proximity sensors could be explained by wild roosting proximity, kinship, or rates of co-feeding, social grooming, and food sharing during 22 months in captivity. We assessed evidence for six hypothetical scenarios of social foraging, ranging from individual to collective hunting. We found that female vampire bats departed their roost individually, but often re-united far outside the roost. Nonrandomly repeating foraging encounters were predicted by within-roost association and histories of cooperation in captivity, even when controlling for kinship. Foraging bats demonstrated both affiliative and competitive interactions and a previously undescribed call type. We suggest that social foraging could have implications for social evolution if ‘local’ cooperation within the roost and ‘global’ competition outside the roost enhances fitness interdependence between frequent roostmates.