Some sheep breeds are naturally prolific, and they are very informative for the studies of reproductive genetics and physiology. Major genes increasing litter size (LS) and ovulation rate (OR) were suspected in the French Grivette and the Polish Olkuska sheep populations, respectively. To identify genetic variants responsible for the highly prolific phenotype in these two breeds, genome-wide association studies (GWAS) followed by complementary genetic and functional analyses were performed. Highly prolific ewes (cases) and normal prolific ewes (controls) from each breed were genotyped using the Illumina OvineSNP50 Genotyping Beadchip. In both populations, an X chromosome region, close to the BMP15 gene, harbored clusters of markers with suggestive evidence of association at significance levels between 1E−05 and 1E−07. The BMP15 candidate gene was then sequenced, and two novel non-conservative mutations called FecXGr and FecXO were identified in the Grivette and Olkuska breeds, respectively. The two mutations were associated with the highly prolific phenotype (pFecXGr = 5.98E−06 and pFecXO = 2.55E−08). Homozygous ewes for the mutated allele showed a significantly increased prolificacy (FecXGr/FecXGr, LS = 2.50±0.65 versus FecX+/FecXGr, LS = 1.93±0.42, p<1E−03 and FecXO/FecXO, OR = 3.28±0.85 versus FecX+/FecXO, OR = 2.02±0.47, p<1E−03). Both mutations are located in very well conserved motifs of the protein and altered the BMP15 signaling activity in vitro using a BMP-responsive luciferase test in COV434 granulosa cells. Thus, we have identified two novel mutations in the BMP15 gene associated with increased LS and OR. Notably, homozygous FecXGr/FecXGr Grivette and homozygous FecXO/FecXO Olkuska ewes are hyperprolific in striking contrast with the sterility exhibited by all other known homozygous BMP15 mutations. Our results bring new insights into the key role played by the BMP15 protein in ovarian function and could contribute to a better understanding of the pathogenesis of women′s fertility disorders. Although causes altering reproductive function and leading to several fertility syndromes in women are various, a clear association between mutations in some members of the TGFβ family (BMP15 and GDF9) and abnormal ovarian phenotype has established the importance of these factors for normal female fertility. Some sheep breeds are naturally prolific since they carry major genes affecting ovulation rate and litter size. These species are therefore unique informative models for the study of reproductive genetics and physiology. Through a GWAS conducted in two sheep breeds using highly prolific ewes as cases and normal prolific ewes as controls, we identified an X chromosome locus close to the BMP15 gene in both breeds. Two novel non-conservative BMP15 mutations, one in each population, located in very well conserved domains of the protein were associated with the phenotype at heterozygous and homozygous status. Moreover, we showed that both mutations altered the BMP15 signaling activity, suggesting a novel kind of BMP15 variant responsible for an atypical high prolificacy, in contrast to all other BMP15 variants described so far. Our findings suggest an additional role of the BMP15 protein in folliculogenesis and could contribute to a better understanding of the pathogenesis of women′s fertility disorders.