Due to their potential impact on the host’s phenotype, organ-specific microbiotas are receiving increasing attention in several animal species, including cattle. Specifically, the vaginal microbiota of ruminants is attracting growing interest, due to its predicted critical role on cows’ reproductive functions in livestock contexts. Notably, fertility disorders represent a leading cause for culling, and additional research would help to fill relevant knowledge gaps. In the present study, we aimed to characterize the vaginal microbiota of a large cohort of 1171 female dairy cattle from 19 commercial herds in Northern France. Vaginal samples were collected using a swab and the composition of the microbiota was determined through 16S rRNA sequencing targeting the V3–V4 hypervariable regions. Initial analyses allowed us to define the core bacterial vaginal microbiota, comprising all the taxa observed in more than 90% of the animals. Consequently, four phyla, 16 families, 14 genera and a single amplicon sequence variant (ASV) met the criteria, suggesting a high diversity of bacterial vaginal microbiota within the studied population. This variability was partially attributed to various environmental factors such as the herd, sampling season, parity, and lactation stage. Next, we identified numerous significant associations between the diversity and composition of the vaginal microbiota and several traits related to host’s production and reproduction performance, as well as reproductive tract health. Specifically, 169 genera were associated with at least one trait, with 69% of them significantly associated with multiple traits. Among these, the abundances of Negativibacillus and Ruminobacter were positively correlated with the cows’ performances (i.e., longevity, production performances). Other genera showed mixed relationships with the phenotypes, such as Leptotrichia being overabundant in cows with improved fertility records and reproductive tract health, but also in cows with lower production levels. Overall, the numerous associations underscored the complex interactions between the vaginal microbiota and its host. Given the large number of samples collected from commercial farms and the diversity of the phenotypes considered, this study marks an initial step towards a better understanding of the intimate relationship between the vaginal microbiota and the dairy cow’s phenotypes.