Teladorsagiosis is a major production-limiting disease in ruminant production in temperate regions throughout the world and one of the key interventions in the management of the disease is the prevention of pasture contamination with Teladorsagia circumcincta larvae by ewes during the periparturient relaxation in immunity which occurs around lambing. Here, we describe the immunisation of twin-bearing ewes with a T. circumcincta recombinant vaccine and the impact that vaccination has on their immune responses and shedding of parasite eggs during a continuous T. circumcincta challenge period spanning late gestation and lactation. In ewes which displayed a clear periparturient relaxation in immunity, vaccination resulted in a 44% reduction in mean cFEC (p = 0.027) compared to control (immunised with adjuvant only) ewes. Recombinant antigen-specific IgG and IgA were detected in the serum of vaccinated ewes following each immunisation and in colostrum taken from vaccinated ewes post-partum. Low levels of antigen-specific IgG were detected in colostrum from control ewes; however the levels of recombinant antigen-specific IgA detected in colostrum from these ewes were similar to those measured in the vaccinated animals. Antigen-specific IgG and IgA levels in blood collected within 48 h of birth from lambs largely reflected those in the colostrum of their ewes.