In this study, we combined RNA-sequence data, genome-wide association studies (GWAS) and imputed sequence data (Daetwyler et al., 2014; Nat. Genet. 46: 858–865) to identify variants associated with dairy cow fertility. We tested the hypothesis that genes differentially expressed in the endometrium and corpus luteum (CL) on d 13 of the estrous cycle between cows with either good (Fert+) or poor (Fert-) genetic merit for fertility, would identify quantitative trait loci (QTL) regions and sequence variants associated with fertility in cattle. After an adjustment for multiple testing (Benjamini and Hochberg, P ≤ 0.05), 9 and 560 genes were differentially expressed in the endometrium and CL, respectively, between Fert+ and Fert– cows. These differentially expressed genes (DEG) identified 93 QTL regions (P < 10⁻³) that were validated by fertility GWAS using high-density genotypes from independent dairy cattle populations in both Australia (16,794 bull and cow genotypes) and Ireland (2,660 bull genotypes), with 54% of the signals detected primarily on BTA18 (23%), 5 (9%), 7 (8%), 8 (8%) and 29 (6%). The QTL regions were primarily associated with genes involved in prostaglandin F_2α (synthesis, secretion and action) and immune-related processes in the endometrium and CL. In addition, genes involved in steroidogenesis and mRNA processing were also identified in the CL. Seventeen sequence variants significantly associated with fertility (P ≤ 10⁻⁵) in the Australian population were identified within 2 kb upstream and downstream of DEG involved in mRNA processing or the immune system. One missense variant (SIFT value = 0.01; i.e., deleterious to protein function) significantly associated with fertility was identified in EIF4EBP3, a gene involved in translation initiation. The results of this study enhance our understanding of (1) the contribution of the endometrium and CL transcriptome to phenotypic reproductive performance; and (2) the genomic architecture influencing a complex trait such as dairy cow reproductive performance.