Mermithid nematodes, such as Ovomermis sinensis, are used as biological control agents against many insect pests, including cotton bollworm (Helicoverpa armigera). However, given the host's robust immune system, the infection rate of O. sinensis is low, thus restricting its widespread use. To understand the host defense mechanisms against mermithid nematodes, we identified and characterized a protein involved in the recognition of O. sinensis, the potential O. sinensis-binding protein C-type lectin 1 (HaCTL1a and/or HaCTL1b), which was eluted from the surface of O. sinensis after incubation with H. armigera plasma. HaCTL1b is homologous to the previously reported HaCTL1a protein. HaCTL1 was predominantly expressed in hemocytes and was induced by the steroid hormone 20-hydroxyecdysone through ecdysone receptor (HaEcR) or ultraspiracle (HaUSP), or both. Binding assays confirmed the interactions of the HaCTL1 proteins with O. sinensis but not with Romanomermis wuchangensis, a parasitic nematode of mosquito. Moreover, the HaCTL1 proteins were secreted into the hemocoel and promoted hemocyte-mediated encapsulation and phagocytosis. A knockdown of HaEcR and/or HaUSP resulted in compromised encapsulation and phagocytosis. Thus, HaCTL1 appears to modulate cellular immunity in the defense against parasitic nematodes, and the 20-hydroxyecdysone-HaEcR-HaUSP complex is involved in regulating the process.