Many bacteria metabolize ethanolamine as a nutrient source through cytoplasmic organelles called bacterial microcompartments (BMCs). In Fusobacterium nucleatum (Fn), an opportunistic anaerobic pathogen linked to adverse pregnancy outcomes, the ethanolamine utilization (eut) system plays a crucial role in adaptation and virulence. The F. nucleatum genome harbors a conserved eut locus with 21 genes encoding enzymes for ethanolamine transport and catabolism, several putative BMC shell proteins, and a two-component signal transduction system (TCS). We demonstrate that ethanolamine induces the expression of eut genes and promotes BMC formation in Fn. This process is transcriptionally regulated by the TCS EutV-EutW, as deletion of the response regulator EutV abolishes eut gene induction and BMC assembly. Mass spectrometry of isolated BMCs identified the structural components EutL, EutM1, EutM2, and EutN, which are essential for proper BMC assembly and function. Deletion of eutN, eutL/eutM1/eutM2, oreutL/eutM1/eutM2/eutN impairs BMC formation and ethanolamine utilization, leading to cell growth defects. Importantly, BMCs also assemble in Fn cultured with placental cells or conditioned media, a process dependent on BMC shell proteins. Notably, eutN deletion results in a significant reduction in Fn-induced preterm birth in a murine model, demonstrating that BMC-mediated ethanolamine metabolism is critical for fusobacterial virulence. To further dissect the role of ethanolamine metabolism in Fn-mediated infection, we examined the function of the eutBC complex, which encodes the ethanolamine ammonia-lyase (EAL). Surprisingly, deletion of eutBC (ΔeutBC) led to a hypervirulent phenotype, characterized by increased bacterial colonization of placental and fetal tissues and severe fetal loss in mice. RNA-seq analysis revealed that infection with the ΔeutBC mutant infection triggers upregulation of oxidative stress response genes (modR, modS, msrAB) and host immune markers associated with macrophage and B-cell activation. Histological analysis further confirmed heightened placental inflammation and tissue degradation. Mechanistically, we found that deletion of eutH, which encodes an ethanolamine transporter, mitigates the severe virulence phenotype of ΔeutBC, suggesting that ethanolamine accumulation drives a compensatory stress response that enhances Fn virulence and immune activation. Together, our findings establish that ethanolamine metabolism and BMC-mediated compartmentalization are critical for Fn pathogenicity. Disrupting these pathways alters bacterial virulence, either attenuating or exacerbating infection outcomes, underscoring the potential of targeting ethanolamine metabolism as a therapeutic strategy to mitigate Fn-associated complications during pregnancy.