Our understanding of the molecular mechanisms by which microorganisms affect animal behavior rests on single-microorganism studies. Yeasts affect Drosophila melanogaster olfactory behavior, yet it is unclear how bacteria or microbe-microbe interactions affect Drosophila behavior. The Drosophila microbiome consists of yeasts, acetic acid bacteria (AAB), and lactic acid bacteria (LAB), which co-occur in fruit and in the Drosophila intestinal tract. Drosophila appears to augment its resident microbiome through feeding, implicating Drosophila behavior in microbiome selection. Beneficial AAB and LAB emit acetic acid and lactic acid, respectively, yet acidity repels Drosophila via a dedicated olfactory circuit. One answer to this paradox is that Drosophila acquires bacterial microbiome members through a passive mechanism, whereas another posits that bacterial microbiome members actively attract Drosophila despite their acidity, either alone or in the context of communities. To distinguish these possibilities, we adapted a behavioral assay and measured Drosophila olfactory preference toward microbiome members grown individually and in communities. Drosophila prefers cultures of microbiome members grown in communities relative to cultures of the same microorganisms grown individually and then mixed, suggesting that Drosophila olfactory behavior is tuned to emergent microbe-microbe interactions. The conserved olfactory receptor Or42b partially mediated Drosophila preference for the two microorganisms grown together (yeast-AAB co-culture) to the same microorganisms grown individually and then mixed. Drosophila co-culture preference correlated with three emergent properties: ethanol catabolism, a unique volatile profile, and yeast population decline. Acetobacter conversion of Saccharomyces-derived ethanol was necessary and acetic acid and its metabolic derivatives were sufficient for Drosophila co-culture preference, supporting the hypothesis that AAB actively attracts Drosophila as part of a microbial community. Additional chemical and behavioral analyses identified acetaldehyde metabolic derivatives as emergent microbial community metabolites that attract Drosophila. In sum, we discovered a molecular mechanism by which a multispecies community affects animal behavior. Our data support a model whereby emergent microbial metabolism cues Drosophila to associate with a diverse, metabolically beneficial microbiome.