Reproductive experience (i.e. pregnancy and lactation) alters a number of physiological and behavioural endpoints, many of which are related to reproductive function and are regulated by oestrogen. For example, reproductive experience significantly attenuates the oestradiol-induced prolactin surge on the afternoon of pro-oestrous and circulating oestradiol levels are reduced at this time. Although parity-related effects on oestrogen receptor (ER) α have been observed within the anterior pituitary, there are currently no data regarding possible parity-induced alterations in ERα in the brain. Thus, the present study aimed to examine the effect of parity on the expression of ERα in reproductively relevant brain regions. Moreover, because previous findings have demonstrated that the long-term effects of reproductive experience are often oestrous cycle-dependent, ERα was examined at two stages of the oestrous cycle (i.e. dioestrous and pro-oestrous). Finally, because the expression of ERα is significantly influenced by age, both young and middle-aged females were included in the present study. ERα status was determined using immunohistochemistry in select brain regions involved in the regulation of reproductive behaviour in age-matched, cycling primiparous (i.e. one pregnancy and lactation) and nulliparous females as well as in age-matched, noncycling (i.e. persistent oestrous) 12 month-old primiparous and nulliparous females. Significant shifts in ERα cell numbers were observed in the medial preoptic area and medial amygdala as a consequence of reproductive experience in an oestrous-dependent manner. These findings indicate that significant changes in ERα activity occur in the brain as a function of reproductive experience.