A cDNA representing the gene Teladorsagia circumcincta apyrase‐1 (Tci‐apy‐1) was isolated, by PCR, from a T. circumcincta fourth‐stage larval (L4) cDNA library. The closest orthologue of this gene is a Ca2+‐dependent apyrase from Ostertagia ostertagi, with 92% amino acid identity across all 339 residues. Tci‐apy‐1 is transcribed in a stage‐specific manner, the transcript being predominant in L4, detectable in the adult cDNA, but absent from eggs and infective third‐stage larvae (L3). The protein, Tci‐APY‐1, was detected by immunoblotting in extracts of L4 nematodes and was present in excretory/secretory products from the same developmental stage. A recombinant version of Tci‐APY‐1 was expressed in bacteria as an active enzyme that hydrolysed nucleoside triphosphate substrates with a preference of ATP over other nucleoside triphosphates. Recombinant Tci‐APY‐1 hydrolysed ATP and ADP but not AMP. Apyrase activity was divalent cation‐dependent, with no hydrolysis in the presence of Mg2+, but activation in the presence of Ca2+. Recombinant Tci‐APY‐1 was bound by IgG present in serum and both IgG and IgA present in abomasal mucus from trickle‐infected, immune sheep but not in material derived from lambs exposed to a single infection. The potential immunomodulatory roles of this Tci‐APY‐1 are discussed in relation to purinergic signalling.