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The queen caste plays a central role in colony success in eusocial insects, as queens lay eggs and regulate colony behavior and development. Queen failure can cause colonies to collapse, which is one of the major concerns of beekeepers. Thus, understanding the biology behind the queen’s health is a pressing issue. Previous studies have shown that the bee microbiome plays an important role in worker bee health, but little is known about the queen microbiome and its functionin vivo. Here, we characterized the queen microbiome, identifying for the first time the present species and their putative functions. We show that the queen microbiome has predicted nutritional and protective roles in queen association and comprises only four consistently present bacterial species. Additionally, we bring to attention the spread of phages in the queen microbiome, which increased in abundance in failing queens and may impact the fate of the colony.