Bacteria colonize specific niches in the animal gut. However, the genetic basis of these associations is often unclear. The protobacterium Frischella perrara colonizes the hindgut of honey bees, where it causes a characteristic immune response leading to the formation of the scab phenotype. Genetic determinants required for the establishment of this specific association are unknown. Here, we isolated three point mutations in the genes encoding the DNA-binding protein integration host factor (IHF). All three mutants formed larger colonies than the wild type in vitro and did not produce an aryl polyene metabolite, which confers a yellow color to F. perrara colonies. Inoculation of microbiota-free bees with one of the mutants drastically decreased gut colonization of F. perrara and abolished scab development. Using RNAseq we find that IHF affects the expression of potential colonization factors, including a colibactin biosynthetic gene cluster, two Type 6 secretion systems, pili genes, and the aryl polyene biosynthesis pathway. Gene deletions of these components revealed different colonization defects. While some mutants were abolished in their capacity to colonize the gut, others colonized but did not trigger the scab phenotype. IHF is conserved across many bacteria and may thus regulate host colonization also in other animal symbionts.