Inflammatory cytokine interleukin-17 (IL-17) binds its receptors (IL-17Rs) to activate the downstream immune signals and plays an important role in host defense. In the present study, an IL-17 receptor (designated as CgIL-17R1) was identified from oyster Crassostrea gigas with an open reading frame of 3141 bp encoding 1047 amino acids. The amino acid sequence of CgIL-17R1 with two conserved FN3 domains shared higher similarity with other known IL-17Rs from mollusc species. The recombinant CgIL-17R1 protein (rCgIL-17R1) displayed high binding affinity to the recombinant CgIL-17 protein (rCgIL-17) in vitro. The mRNA transcripts of CgIL-17R1 were significantly higher expressed in haemocytes, especially in granunolyctes, compared with that in other tissues. After the stimulation with Vibrio splendidus or rCgIL17-1 in vivo, the expressions of CgIL-17R1 and cell proliferation related genes (CgRunx-1, CgCDC-6, CgCDC-45, and CgCDK-2) were significantly up-regulated in haemocytes (p < 0.01). When the CgIL-17R1 expression was interfered by specific CgIL-17R1-dsRNA, the expressions of these cell proliferation related genes reduced significantly, and the proliferation rate of haemocytes declined dramatically at 6 h post V. splendidus stimulation (p < 0.01), compared to that of blank group. These results collectively indicated that CgIL-17R1 expressed in granulocytes mediated the CgIL-17 induced haemocytes proliferation during immune response in oyster C. gigas, which provided novel information about the regulation of haemocyte proliferation in invertebrates.