Stressor‐induced elevation of circulating cortisol levels is generally considered to have an inhibitory effect on reproduction in teleosts. However, mature female fish have higher levels of circulating cortisol levels, and this is particularly telling in salmonids during their spawning migration. This raises the possibility that a cortisol buffering capacity is active at the level of the gonad. This is particularly important given the recent findings in zebrafish (Danio rerio, Cyprinidae) that zygotic cortisol content, either high or low, can alter developmental programming. Therefore, a tight regulation of corticosteroid during oogenesis may be essential for proper ovarian development. Here, we focus on the temporal dynamics of cortisol in the ovary and its role in regulating the different processes related to oogenesis. Maternally deposited cortisol along with the local production of this steroid by the ovary may be involved in the regulation of oogenesis. We propose two critical stages when cortisol may exert a modulatory effect on oogenesis. The first stage occurs during vitellogenesis when maternal cortisol is incorporated into the yolk, and the second is during maturation and ovulation when cortisol may have a regulatory role on the action of maturation‐inducing hormones. A key protective mechanism to prevent excess cortisol deposition appears to be the upregulation of 11β‐hydroxysteroid dehydrogenase 2 in the theca and/or granulosa cells of the developing oocyte in response to excess maternal cortisol stimulation. Taken together, cortisol dynamics during oogenesis is complex, but maintaining a “Goldilocks” concentration of this steroid may be a critical process governing successful spawning and progeny development.