Significance Virtually all animals are associated with symbiotic bacteria. How these associations are modulated across an animal’s life cycle is a key question in understanding animal–bacteria interactions, particularly in organisms that undergo metamorphosis during development. Here, we used the cereal weevil to show how symbiosis is reorganized during metamorphosis, a developmental process entailing drastic tissue rearrangements. In this insect, symbionts are housed within specialized host cells, the bacteriocytes, that form the bacteriome tissue. We show that the bacteriome is completely remodeled during metamorphosis through host–symbiont communication, involving adhesion and motility host proteins and a temporary symbiont infectious behavior. This interkingdom dialogue results in the adaptation of the bacteriome to adulthood, highlighting the intertwining of symbiosis with host development.