Maternal hypothalamic‐pituitary‐adrenal axis activity may prenatally program sex‐specific stress‐response pathways. We investigated associations between maternal cortisol during pregnancy and infant parasympathetic responsivity to stress among 204 mother–infant pairs. Cortisol indices included 3rd trimester hair cortisol, as well as diurnal slope and area under the curve, derived from saliva samples collected during pregnancy. Mother–infant dyads participated in the Repeated Still‐Face Paradigm (SFP‐R) at age 6 months. We calculated respiration‐adjusted respiratory sinus arrhythmia (RSAc), an indicator of parasympathetic activation, from infant respiration and cardiac activity measured during the SFP‐R. We used multivariable linear mixed models to examine each cortisol index in relation to infant RSAc and investigated sex differences using cross‐product terms. Diurnal cortisol indices were not associated with RSAc. There was no association between hair cortisol and baseline RSAc. However, hair cortisol was associated with sex‐specific changes in RSAc over the SFP‐R such that, among girls, parasympathetic withdrawal was reduced with increasing prenatal exposure to cortisol. Consistently higher levels of prenatal cortisol exposure may lead to dampened parasympathetic responsivity to stress during infancy, particularly among girls. Maternal hair cortisol may be particularly valuable for studying the effects of prenatal cortisol exposure on infant autonomic reactivity.