In this study, we identify and characterize a novel phage-inducible chromosomal island (PICI) found in commensal Escherichia coli MP1. This novel element, EcCIMP1, is induced and mobilized by the temperate helper phage vB_EcoP_Kapi1. EcCIMP1 contributes to superinfection immunity against its helper phage, impacting bacterial competition outcomes. Genetic analysis of EcCIMP1 led us to uncover a putative transcriptional repressor, which silences virulence gene expression in the murine pathogen Citrobacter rodentium. We also found a putative excisionase encoded by EcCIMP1 which paradoxically does not promote excision of EcCIMP1 but rather supports excision of the helper phage. Another putative excisionase encoded by a presumed integrative conjugative element can also support the excision of vB_EcoP_Kapi1, demonstrating crosstalk between excisionases from multiple classes of mobile genetic elements within the same cell. Although phylogenetically distant from other characterized PICIs, EcCIMP1 and EcCIMP1-like elements are prevalent in both pathogenic and commensal isolates of E. coli from around the world, underscoring the importance of characterizing these abundant genetic elements.