Traditional antibody generation requires purified antigens, a months-long bottleneck that fails to reproduce native surface antigen display. We eliminate this constraint by reprogramming Citrobacter rodentium into a self-contained platform: engineered strains biosynthesise heterologous antigens during infection, simultaneously evaluating immunogenicity and generating functional polyclonal antibodies in 28 days. C. rodentium's IgG-dependent clearance kinetics naturally drive physiological humoral maturation, and its Type III Secretion System (T3SS) effector proteins provide a toolbox to tune host-pathogen interactions to optimise mucosal antigen presentation and rescue fitness defects. Our platform, citrOgen, combines three engineering strategies: (i) plug-and-play operon substitution for complex polysaccharides (LPS, capsule), (ii) T3SS effector augmentation (EspO effector overexpression) to maintain colonisation despite heterologous expression costs, and (iii) infection-stage promoters (T3SS-regulated) for controlled protein complex assembly. Applied to WHO critical priority pathogens (Klebsiella pneumoniae, E. coli ST131), single genome edits produced functional antibodies within 35 days. Functional validation demonstrated research and diagnostic utility: antibodies enabled in vivo evaluation of antigen protective capacity (preventing lethal K. pneumoniae pneumosepsis organ failure across haematological, lung, and renal markers), inhibited type 3 fimbrial biofilm formation and enabled high-throughput serotyping of 100 diverse clinical isolates. Critically, citrOgen bypasses antigen production entirely while preserving native conformations, accelerating antigen prioritisation for vaccine development and generating diagnostic reagents. This chassis engineering approach addresses a major bottleneck in antibody-based research tools for antimicrobial resistance, offering a scalable genetics-to-antibody pipeline that accelerates both target validation and diagnostic development against Gram-negative priority pathogens.