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Over the past decade, small RNA technologies have been proposed for improved control of parasitic worms. Although achievements have been made in the identification of target candidates and in the improvement of reverse genetic tools, few of those have been tested in domestic animals. In this work, crucial genes (i.e., daf-9/cyp-22a1 , bli-5 and HCON_00083600 ) involved in the developmental transition (i.e., activation, moulting and haem utilisation) from the infective L3 stage to the parasitic L4 stage of Haemonchus contortus (the barber’s pole worm commonly found in small ruminants) in vitro were identified and verified using RNA interference (RNAi) technologies during the adaptation to parasitism of this parasite in vivo. Silencing each of the daf-9/cyp-22a1 , bli-5 and HCON_00083600 genes in the infective larvae of H. contortus resulted in compromised larval development and viability in vitro, and silencing of either the daf-9/cyp-22a1 , bli-5 or HCON_00083600 gene led to a marked reduction in the faecal egg count and worm burden in sheep. In conclusion, the results demonstrate that genes involved in larval activation, moulting and haem utilisation of H. contortus are target candidates, and the application of RNAi technologies for better control of these and related parasitic nematodes is promising, preferably with an improved RNAi tool for efficient and long-lasting effects in host animals.