We hypothesised that the superior reproductive performance in cows with high genetic merit for fertility is, in part, explained by a better follicular environment resulting in high quality oocytes. To test this, trans-vaginal ovum-pickup was used to collect preovulatory cumulus-oocyte complexes and follicular fluid from spring-calving primiparous Holstein-Friesian dairy cows with either low (n = 23) or high (n = 26) genetic merit for fertility. Only cows in their second or third oestrus were sampled, (62 ± 17 days postpartum). Multiplex quantitative PCR was used to measure the expression of gene markers of oocyte quality in the cumulus cell masses and oocytes. High performance liquid chromatography was used to measure the concentration of amino acids, steroids, and metabolites in the follicular fluid and plasma. Compared with low fertility cows, oocytes from high fertility cows had higher expression of gene markers for good oocyte quality (HAS2, VCAN, PDE8A, P < 0.05). The follicular environment of these cows was also markedly different, with lower concentrations of serine, proline, methionine, and isoleucine than cows with low genetic fertility (P < 0.05). High fertility cows also tended to have lower (P = 0.053) follicular fluid concentrations of non-esterified fatty acids than cows with low genetic fertility. Plasma concentrations of asparagine, alanine, proline, tyrosine, methionine, and phenylalanine were lower in high fertility cows than low fertility cows. High non-esterified fatty acids concentrations are reportedly harmful to the developing oocyte, suggesting the follicular fluid composition of low fertility cows may be detrimental to oocyte quality. These differences in gene expression and follicular fluid constituents are consistent with cows with high genetic merit for fertility producing higher quality oocytes than cows with low genetic merit for fertility and this may be related to an altered follicular environment.