Environmental factors can shape reproductive investment strategies and influence the variance in male mating success. Environmental effects on extrapair paternity have traditionally been ascribed to aspects of the social environment, such as breeding density and synchrony. However, social factors are often confounded with habitat quality and are challenging to disentangle. We used both natural variation in habitat quality and a food supplementation experiment to separate the effects of food availability—one key aspect of habitat quality—on extrapair paternity (EPP) and reproductive success in the black-throated blue warbler, Setophaga caerulescens. High natural food availability was associated with higher within-pair paternity (WPP) and fledging two broods late in the breeding season, but lower EPP. Food-supplemented males had higher WPP leading to higher reproductive success relative to controls, and when in low-quality habitat, food-supplemented males were more likely to fledge two broods but less likely to gain EPP. Our results demonstrate that food availability affects trade-offs in reproductive activities. When food constraints are reduced, males invest in WPP at the expense of EPP. These findings imply that environmental change could alter how individuals allocate their resources and affect the selective environment that drives variation in male mating success.