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Estrogen receptor alpha (ERα) typically masculinizes male behavior, while low levels of ERα in the medial amygdala (MeA) and the bed nucleus of the stria terminalis (BST) are associated with high levels of male prosocial behavior. In the males of the highly social prairie vole (Microtus ochrogaster), increasing ERα in the MeA inhibited the expression of spontaneous alloparental behavior and produced a preference for novel females. To test for the effects of increased ERα in the BST, a viral vector was used to enhance ERα expression in the BST of adult male prairie voles. Following treatment, adult males were tested for alloparental behavior with 1–3-day-old pups, and for heterosexual social preference and affiliation. Treatment did not affect alloparental behavior as 73% of ERα-BST males and 62.5% of control males were alloparental. Increasing ERα in the BST affected heterosexual affiliation, with ERα-BST males spending significantly less total time in side-by-side contact with females relative to time spent with control males. ERα-BST males did not show a preference for either the familiar or novel female. These findings differed significantly from those reported in ERα-MeA enhanced males, where ERα inhibited alloparental behavior and produced a preference for a novel female. The findings from this study suggest two things: first, that increased ERα in the BST decreases social affiliation and second, that altering ERα in different regions of the social neural circuit differentially impacts the expression of social behavior.