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Production of the auxin indole-3-acetic acid (IAA) has been demonstrated for bacterial isolates from plant leaf surfaces, but its prevalence and contribution to phyllosphere fitness are not well understood. We took a multipronged approach to reveal the abundance, identity, and activity of IAA-producing bacteria from the foliage of field-grown lettuce. Among 235 early- and late-season isolates that were tested, 45% scored as high producers of IAA in culture. Most belonged to Pantoea, Erwinia, or other genera in the Enterobacterales, whereas the majority of low/no IAA-producing isolates were Arthrobacter species. Bray-Curtis similarity was high between subsets of isolates with high IAA-producing ability and isolates with the greatest abundance late in the growing season, hinting at a positive relationship between IAA production and phyllosphere fitness. Whole-genome sequencing of selected high and low/no IAA-producing strains revealed canonical ipdC genes for IAA production in high (Rahnella, Erwinia) as well as low/no (Winslowiella, Serratia) IAA producers. One of the high IAA-producing isolates (Pseudarthrobacter) carried a gene with coding similarity to a clade of IaaM-like proteins for which a role in IAA biosynthesis has been suggested but not yet experimentally confirmed. Using an IAA-responsive, green fluorescent protein-based bioreporter, we found that bacteria produce IAA on leaf surfaces and that phyllosphere conditions induce IAA production. The finding that IAA production is common among bacterial phyllosphere colonizers invites a closer look at the benefits of IAA production for bacterial survival on plant leaf surfaces. [Figure: see text] Copyright © 2025 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.