Cigarette smoke is a well known ovotoxicant which has been linked to premature ovarian failure in offspring exposed in utero.  Despite an increased awareness of the adverse effects of cigarette smoke exposure on systemic health, over 37% of Australian mothers under the age of 25 smoke during pregnancy highlighting the need for further research into how maternal smoking effects offspring fertility. In this study we treated pregnant mice with mainstream cigarette smoke via direct inhalation over the gestational/suckling period to mimic human exposure, and examined the ovarian development and fertility of their female offspring. Histomorphological analysis revealed a 2-fold decrease (p<0.05) in primordial follicle numbers in juvenile females. Caspase activity and DNA damage were also detected in developing follicles but were absent from primordial follicles. Interestingly primordial follicles in smoke-exposed offspring were positive for markers of follicular activation, results which are consistent with our previous findings for ovaries of directly smoked females. Defects in ovarian function persisted in adulthood, with increased levels of mitochondrial ROS (~2 fold) and lipid peroxidation (~1.8 fold) which was associated with a 40% decrease (p<0.05) in sperm egg binding. Our results demonstrate that maternal cigarette smoke exposure during the gestational and suckling period causes depletion of the primordial and small growing follicle pool and eggs that do reach maturity are under oxidative stress which results in reduced fertilisation potential.