Humans have historically relied on acetic acid bacteria (AAB) for food fermentation, yet their origins must trace back to free-living species outside of human environments. In nature, plants, fruit flies, and social insects host AAB. However, the evolutionary transitions of AAB from symbiotic hosts to fermented foods remain ambiguous. Here, we conduct a comprehensive phylogenomic analysis of 570 publicly available AAB genomes. We find that the ∼170My evolutionary history of this group is concordant with the rise of angiosperms, corbiculate bees, and the consequential accelerated availability of environmental carbohydrates. Unlike other ferment-associated microbes, ferment-associated AAB have exclusively evolved from clades inhabiting flowers and fruits, but not insect hosts. Genomic features are similar in plant- and ferment-associated AAB, yet markers of early adaptation to ferments are also present. Conversely, social insect-associated AAB have reduced genome sizes, which may have limited their functional capability to disperse into ferments. Plant- and ferment-associated AAB coincide in the ability to metabolise diverse plant carbohydrates, though both have adapted to produce habitat-specific carbohydrate-active enzymes. In contrast, metabolic capacity is reduced in social insect-associated AAB. By tracing the phylogenomics of this clade, we understand how evolution forged AAB capable of performing metabolic work for humans, shaping the history and potential futures of fermentation. ### Competing Interest Statement The authors have declared no competing interest.
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