The biology and vectorial capacity of haematophagous ticks are directly related to effective blood feeding and digestion. The midgut-associated proteases in ticks are involved in the blood (Hb) digestion cascade, the molecular mechanisms of which are yet poorly understood. Our previous studies indicated that Haemaphysalis longicornis midgut-specific asparaginyl endopeptidases/legumains, HlLgm and HlLgm2, act in the Hb digestion cascade. Here, we investigated the potential of these enzymes in blood feeding and digestion, midgut remodelling and reproduction of ticks by employing RNA interference (RNAi) techniques. Injection of HlLgm- and HlLgm2 gene-specific double-stranded RNAs into unfed adult female H. longicornis caused gene-specific transcriptional and translational disruptions. RNAi impacted on tick blood feeding leading to death of the feeding ticks, failure of ticks to reach repletion and significant reductions in engorged tick body weight. Histological examination revealed that deletion of legumains resulted in damage to the midgut tissues and disruption of normal cellular remodelling during feeding. Gene knock-down also caused significantly delayed onset of oviposition, reduced number of eggs and, most strikingly, structurally deformed eggs that failed to hatch suggesting imperfect embryogenesis. Synergistic impacts of RNAi were reflected on all parameters evaluated when HlLgm and HlLgm2 were silenced together. These findings suggest that legumains may play modulatory roles in blood feeding and digestion, midgut cellular remodelling and embryogenesis in H. longicornis. Deletion of legumains in H. longicornis would help in controlling the tick population and thereby transmission of diseases to their hosts.