The f1 bacteriophage is a circular single-stranded DNA filamentous virus that infects bacterial cells containing an F-like conjugative plasmid. Given the ease of genome engineering and high tolerance to protein/peptide display on the capsid, this phage has been employed extensively for various applications, including bio-panning, diagnostics, vaccines and nanomaterials. These applications are made possible by six decades of accumulated knowledge of the phage-host interactions. However, all previous experiments were conducted in bulk cultures, providing only an averaged view of the phage-host interactions and masking the heterogeneity and dynamics at the single-cell level. Here, we inserted a gfp-encoding gene into the f1 genome, ensuring that only the f1-infected Escherichia coli exhibit green fluorescence. Using the engineered reporter phage, we can visualize and track the progress of f1 infection in E. coli in a microfluidic device, enabling quantification of growth rates for both infected and non-infected cells at single-cell resolution. Contrasting with the classical view of the f1 phage as non-lytic and chronically infecting E. coli, we observed that a subpopulation of the culture is killed upon f1 infection, with the degree of lethality varying across different genetic backgrounds. Using the GFP-expressing reporter phage, we are also able to enrich f1-infected cells for downstream phenotypic characterization, such as spread of antimicrobial resistance genes through conjugation and susceptibility to subsequent phage attack, as well as for structural studies of phage assembly. Overall, our study provides novel insights into phage-host interactions and paves the way for innovative application of the f1 phage system.