Biological invasions can alter direct and indirect interactions between species, generating far-reaching changes in ecological networks that affect key ecological functions. We used model and real fruit assays to show that the invasion and formation of high-density supercolonies by the yellow crazy ant (YCA), Anoplolepis gracilipes, disrupt frugivory by endemic birds on Christmas Island, Indian Ocean. The overall handling rates of model fruits by birds were 2.2-2.4-fold lower in ant-invaded than in uninvaded rainforest, and pecking rates by two bird species declined by 2.6- and 4.5-fold, respectively. YCAs directly interfered with frugivory; their experimental exclusion from fruiting displays increased fruit handling threefold to sixfold, compounding indirect effects of ant invasion on resources and habitat structure that influence bird abundances and behaviours. This invasive ant, whose high densities are sustained through mutualism with introduced scale insects, rapidly decreases fruit handling by endemic island birds and may erode a key ecological function, seed dispersal. Because most other invasive ant species form expansive, high-density supercolonies that depend in part on association with hemipteran mutualists, the effects that we report here on avian frugivore-plant associations may emerge across their introduced ranges.