Prophages are viruses that integrate into the genomes of bacteria, which then become lysogens. Lysogens are abundant in the gut of animals, where prophages are known to influence their metabolic pathways and other traits. However, the potential influence of prophages on the gut microbiota-host immune axis in animals remains poorly understood. Here, we investigated the influence of prophages in a marine lysogen,Shewanella fidelis3313, a prevalent member of the gut microbiome of the model tunicate,Ciona robusta. Two prophages, SfPat and SfMu1, were deleted individually and in combination using homologous recombination to observe the effects of these prophages on processes involved in gut colonization. We report here that in vitro, these prophages enhance motility and negatively impact biofilm formation ofS. fidelis 3313. To understand the in vivo impact of these prophage-induced changes in bacterial traits, we exposed metamorphic stage 4Cionajuveniles (the stage that correlates to first feeding and subsequent gut colonization) to both wildtype (WT) and modified strains ofS. fidelis 3313. When colonizing theCionagut, the WT strain experiences an upregulation ofpdeB, a phosphodiesterase known to degrade cyclic di-GMP, a dinucleotide messenger that can positively influence biofilm formation while negatively regulating motility. WT colonization and upregulation ofpdeBalso correlates to a downregulation of theCionagut immune effector, VCBP-C. This study reveals an influence of prophages on bacterial traits and host immune response in the gut of a model organism. Our findings highlight the importance of interkingdom signaling between prophages, bacteria, and their animal hosts in regulating the gut microbiota-host immune axis.