The extra-pair (EP) mating system of birds may be influenced by food resources, such that nutritionally stressed females are unable to pursue EP fertilizations (constrained female hypothesis; CFH), or that females on poor territories acquire EP fertilizations during extra-territorial forays in search of food (mating opportunity hypothesis; MOH). Edges of urban habitat fragments are sites of apparent high food abundance for spotted towhees (Pipilo maculatus), and we used distance to habitat edge in four urban parks in Portland, OR, USA (2004-2006), to test the CFH and MOH. EP paternity was independent of park identity and year; 44% of nests contained EP young and 26% of all young were EP. As predicted by the CFH, EP paternity was more common in nests of long-tailed (presumably) high quality females. However, independently of tail length, younger females had more EP young than older females, a finding consistent with the MOH. Contrary to predictions of both hypotheses, the probability that a nest contained EP young was highest both at the habitat edge and habitat interior while the proportion of young in nests of EP origin (for nests with EP young) was highest at intermediate distances from habitat edge. We propose that high frequency of EP paternity among females in the interior occurred because, as predicted by the MOH, they ranged more widely in search of food and often encountered EP males. High probability of EP paternity near edges was likely unrelated to female quality. Instead, anthropogenic food sources may have attracted individuals to edges and increased encounters between potential EP mates. Simple opportunity seems likely to account for patterns of EP paternity in spotted towhees, suggesting that human altered environments have the potential to substantially affect EP mating behavior.