Beyond the established oral-gut axis links in inflammatory bowel disease (IBD), this review provides an in-depth mechanistic analysis of how specific oral pathobionts disrupt the five intestinal barriers, microbial, chemical, physical, immune, and vascular, driving disease pathogenesis through distinct yet synergistic mechanisms. We synthesize evidence that key pathogens (e.g., Fusobacterium nucleatum (Fn), Porphyromonas gingivalis (Pg)) orchestrate multistep pathogenesis: ectopic translocation followed by targeted barrier disruption, Fn degrading tight junctions, Pg eroding mucus via gingipains, and Klebsiella spp. hijacking T helper 1 cells (Th1) immunity. This pathogen-centric taxonomy reveals pathophysiological sequences: mucosal invasion by Fn precedes microbiota dysbiosis, while Pg virulence factors directly compromise vascular integrity, decoupling translocation routes from barrier-specific outcomes. Notably, we characterize how barrier-specific damage generates therapeutic targets: mucus restoration counters Pg enzymatic degradation, toll-like receptor 4 (TLR4) blockade inhibits Klebsiella-driven inflammation, and Fusobacterium adhesin A (FadA) inhibition prevents Fn endothelial invasion, transitioning from associative findings to mechanism-based interventions. By integrating spatially resolved mechanisms across barrier layers, this work establishes a conceptual framework: oral pathogens act as “barrier disruptors” whose targeted neutralization may improve the IBD disease trajectory. This mechanistic framework positions oral barrier disruption as a druggable axis in IBD, offering actionable biomarkers and microbiota-directed therapeutic strategies.