Methylmercury is a globally distributed pollutant and upper trophic level aquatic fauna are at particularly high risk of exposure. Although methylmercury is known to have a number of neurological and developmental effects, relatively little is known about effects on endocrine disruption and reproduction in aquatic fauna, particularly in response to chronic exposure at low concentrations. We experimentally exposed captive white ibises for 3.5 years (2005–2008) to dietary methylmercury at three environmentally relevant concentrations (0.05, 0.1 and 0.3ppm wet weight in diet). We measured fecal concentrations of estradiol and testosterone metabolites in two consecutive breeding seasons (2007 and 2008). When effects were controlled for stage of breeding, this resulted in altered estradiol and testosterone concentrations in adult breeders of both sexes. Changes in endocrine expression were not consistent over both years, and a clear dose–response relationship was not always present. Endocrine changes were, however, associated at all dose levels with changes in reproductive behavior, reduced reproductive success and altered mate choice in males. Male–male pairing and altered courtship behavior in males were related both to dose treatment and, in 2008, to a demasculinized pattern of endocrine expression. Changes in hormone concentrations of dosed homosexually paired males, when present, were in the same direction but at a higher magnitude than those in heterosexual dosed males. Dosed homosexual males showed decreased testosterone during nest-building and elevated testosterone during incubation when compared with their dosed heterosexual counterparts during the 2008 breeding season. In the same year, exposed males had elevated estradiol during courtship, but had decreased estradiol during other stages in comparison with controls. Dosed females generally showed decreased estradiol and testosterone concentrations compared to controls, albeit not with a clear dose–response effect. Our findings suggest that endocrine disruption due to chronic exposure to even low concentrations of dietary methylmercury may be a widespread mechanism by which reproduction is impaired in wild bird populations.