Temperate phages can be seen as built-in architects, having a tremendous capacity to shape the ecology and evolution of microbial communities. With their possibility of entering lytic or lysogenic replication, they can either erase specific bacterial lineages or rewire the biology of their bacterial host. Temperate phages are found in at least half of all bacteria composing the gastrointestinal microbiome and thus can influence the microbiome by switching between replication strategies. One example is P2-like phages that infect strains from 127 different host genera, including clinically relevant strains of Escherichia coli and Salmonella. Thereby, the SOS response pathway induces a subpopulation of those P2 phages to switch from lysogenic to lytic replication. The SOS pathway can be activated by several stimuli present throughout the intestine. Therefore, P2 phages are recurrently exposed to induction stimuli in the gut, which opens the question of whether temperate phage P2 adjusts the lytic and lysogenic decision-making threshold because of recurrent stress exposure. We can show that induced P2 can infect and re-integrate into the genome of an E. coli mutant genetically cured of its phage. During such autologous infections, we revealed that the number of phages entering lysogenic replication decreases with each round of induction and infection. Furthermore, induced P2 selects for hosts carrying a mutation in the pdeI gene encoding for a c-di-GMP-phosphodiesterase, which is involved in regulating the c-di-GMP concentration. C-di-GMP is a bacterial secondary messenger that controls core bacterial processes like growth, metabolism, and stress response. We combine synthetic biology and experimental evolution to test if previous stress encounters prime future phages’ reactions by evolving replication strategies or selecting a host subpopulation adjusted to endure in a challenging environment, thus securing phage persistence in the microbiome and modulating the microbial community.