Mammals adapt their physiology according to seasons via photoperiodic changes in circulating melatonin. Thus, melatonin regulates reproductive activity through a pituitary-hypothalamic network involving thyroid stimulating hormone subunit b (TSHb) in the pars tuberalis (PT), type 2 (DIO2) and 3 (DIO3) thyroid hormone deiodinases in the tanycytes and RF-amides in the hypothalamus. During gestation, maternal melatonin reaches the fetus via the placenta and affects offspring photoperiodic responses. We tested whether photoperiodic changes in maternal melatonin are capable to program fetal hypothalamic regions controlling seasonal physiology and whether this programming occurs via histogenic mechanisms. Pregnant female Siberian hamsters (Phodopus sungorus) were placed until pups’ weaning under long (LP: 16h light (L):8h dark (D)) or short (SP: 8L:16D) photoperiod. At weaning, on postnatal day 21 (P21), half of the animals from both groups were transferred to intermediate photoperiods (IP) (14L:10D). Male pups were sampled at birth (P0), during lactation (P15), three days after weaning (P24) and at adulthood (P50). Expression of PT TSHß in newborns from dams maintained in SP as compared to LP was strongly downregulated. Consequently, maternal gestation in SP dramatically reduced the newborn’s Dio2/Dio3 ratio, indicative of low hypothalamic T3. At this age, the hypothalamus presented an intense histogenic capacity. After the transfer to IP, there was a strong change in the expression of deiodinases only in SP gestated animals suggesting a profound alteration of the hypothalamic thyroid system by the photoperiodic maternal melatonin signal. In adults kept under IP, the Dio2/Dio3 ratio was lower in SP gestated animals compared to LP, indicating that the early life influence is long-term maintained, affecting reproductive physiology even at an age where hypothalamic histogenic capacity had dramatically decreased. These results indicate that the photoperiodic pituitary-hypothalamic network is functional before birth transducing in utero maternal melatonin which influences hypothalamic offspring´s gene expression through development.