Biotic interactions among commensal members of mammary gland (MG) microbiota play a crucial role in shaping the overall structure of the MG microbiome and determining its functional properties such as stability and resistance to pathogen invasion. The main objectives of the current study were to a) characterize bacterial communities that inhabit different ecological niches of the MG, b) determine their potential associations with the inflammatory status of the udder, and c) characterize niche-specific microbial relationships that are influential in shaping the biodiversity of the MG. To this end, aseptic quarter milk (n = 144) and teat canal swab (n = 144) samples were collected from dairy cows with a wide range of MG inflammatory status, as determined by somatic cell counts (SCC) of the milk, and subjected to genomic DNA extraction and high-throughput 16S rRNA gene sequencing of the V1-V2 hypervariable regions. The teat canal ecosystem was composed of a more diverse and compositionally distinct (P_(PERMANOVA) < 0.001) microbiota compared with the milk. This, coupled with identification of a large number of bacterial lineages that were exclusive to the teat canal microbiota suggested that milk ecosystem act as a potent selective force that precludes the growth of certain environmental bacterial lineages. Further, by utilizing correlation network analysis (CoNet), we identified candidate foundation taxa that showed disproportionately large impact on the structure and diversity of the MG microbiota. These foundation taxa consisted of 2 groups of phylogenetically distinct lineages within the phylum Bacteroidetes showing either positive (unclassified Bacteroidaceae) or negative (Sphingobacterium) correlation with biodiversity metrics of the MG. Certain species within the latter group also showed significant (P < 0.05) positive association with the SCC of the milk. Overall, our results provide novel insights into the biotic interactions that exist among the commensal microbiota of the MG and their potential role in modulating udder health status.