Neurovascular coupling (NVC) is mediated via nitric oxide signaling, which is independently influenced by sex hormones and exercise training. Whether exercise training differentially modifies NVC pre- versus postpuberty, where levels of circulating sex hormones will differ greatly within and between sexes, remains to be determined. Therefore, we investigated the influence of exercise training status on resting intracranial hemodynamics and NVC at different stages of maturation. Posterior and middle cerebral artery velocities (PCA_v and MCA_v) and pulsatility index (PCA_PI and MCA_PI) were assessed via transcranial Doppler ultrasound at rest and during visual NVC stimuli. <i>N</i> = 121 exercise-trained (males, <i>n</i> = 32; females, <i>n</i> = 32) and untrained (males, <i>n</i> = 28; females, <i>n</i> = 29) participants were characterized as pre (males, <i>n</i> = 33; females, <i>n</i> = 29)- or post (males, <i>n</i> = 27; females, <i>n</i> = 32)-peak height velocity (PHV). Exercise-trained youth demonstrated higher resting MCA_v (<i>P</i> = 0.010). Maturity and training status did not affect the ΔPCA_v and ΔMCA_v during NVC. However, pre-PHV untrained males (19.4 ± 13.5 vs. 6.8 ± 6.0%; <i>P</i> ≤ 0.001) and females (19.3 ± 10.8 vs. 6.4 ± 7.1%; <i>P</i> ≤ 0.001) had a higher ΔPCA_PI during NVC than post-PHV untrained counterparts, whereas the ΔPCA_PI was similar in pre- and post-PHV trained youth. Pre-PHV untrained males (19.4 ± 13.5 vs. 7.9 ± 6.0%; <i>P</i> ≤ 0.001) and females (19.3 ± 10.8 vs. 11.1 ± 7.3%; <i>P</i> = 0.016) also had a larger ΔPCA_PI than their pre-PHV trained counterparts during NVC, but the ΔPCA_PI was similar in trained and untrained post-PHV youth. Collectively, our data indicate that exercise training elevates regional cerebral blood velocities during youth, but training-mediated adaptations in NVC are only attainable during early stages of adolescence. Therefore, childhood provides a unique opportunity for exercise-mediated adaptations in NVC.<b>NEW & NOTEWORTHY</b> We report that the change in cerebral blood velocity during a neurovascular coupling task (NVC) is similar in pre- and postpubertal youth, regardless of exercise-training status. However, prepubertal untrained youth demonstrated a greater increase in cerebral blood pulsatility during the NVC task when compared with their trained counterparts. Our findings highlight that childhood represents a unique opportunity for exercise-mediated adaptations in cerebrovascular hemodynamics during NVC, which may confer long-term benefits in cerebrovascular function.