Maternal nutritional intake, such as folate and folic acid supplementation, during pregnancy may affect offspring bone health during childhood. We aimed to determine the associations between maternal dietary and supplementary folate intake and offspring bone health measures, including fracture risk. Data were obtained from 160 of 475 mother–child pairs who had returned for the 11-year follow up of the Vitamin D in Pregnancy Study, an observational cohort study. Incident fractures were ascertained from radiological records and dual X-ray absorptiometry was used to measure bone mineral density and content at 11 years of age. Maternal dietary folate intake during pregnancy was determined by Food Frequency Questionnaire and folate supplementation was determined through self-report. Both measures were undertaken at recruitment (before 16 weeks gestation) and at 28–32 weeks’ gestation. Multivariable linear regression models and Cox regression models were used to examine associations. Results are presented as per 1000 µg folate for dietary measures. There were significant associations between maternal folate supplementation in early pregnancy (< 16 weeks gestation) and offspring spine bone mineral content (BMC) (β = 1.53, 95% CI 0.21, 2.86), spine area (β = 1.10, 95% CI 0.37, 1.82) and total body less head area (β = 329.30, 95% CI 3.50, 55.20) at the 11-year follow-up. The association between spine BMC was attenuated after adjustment for bone size (β = 0.13 95% CI − 0.85, 1.10). There was no association between maternal folate supplementation at 28–32 weeks’ or maternal dietary intake at either time point with any offspring bone outcome. These data suggest that folate supplementation in early pregnancy may be associated with offspring bone size, but not other bone measures.