The mammalian host employs multiple layers of physical and chemical defenses to restrict invading pathogens, creating bottlenecks that limit microbial colonization. However, pathogenic microbes possess virulence factors that allow them to evade these defenses and establish infection. Enteric bacterial pathogens pose a significant global disease burden, with some capable of invading intestinal tissue and disseminating to other organs, leading to severe outcomes such as organ damage, sepsis, and death. Despite this, the population dynamics underlying invasive bacterial infections remain poorly understood.Yersinia pseudotuberculosis (Y. ptb), a Gram-negative pathogen related to Y. pestis, infects the human gastrointestinal tract and can cause severe disease in immunocompromised hosts. As a naturally rodent-adapted pathogen, Y. ptb infection in mice serves as a model for severe human disease. Using a novel barcoded Y. ptb library and the Sequence Tag-based Analysis of Microbial Populations in R (STAMPR) system, we identify a severe restriction in Y. ptb clones from inoculation to intestinal colonization and tissue invasion following oral infection. We find that intestinal colonization bottlenecks are influenced by inoculation method and the endogenous microbiota, whereas tissue invasion remains tightly restricted regardless of these factors. Additionally, we demonstrate that the luminal Y. ptb population is dynamic, with Y. ptb clones shed in stool fluctuating over the course of infection. We find that the tight bottleneck for Y. ptb invasion is partially mediated by TNF signaling, as TNFR1-deficient mice harbor more unique Y. ptb clones at each infection site. Notably, TNF signaling contributes to the containment of Y. ptb within intestinal pyogranulomas, which in immunocompetent mice remain clonal and do not disseminate. Furthermore, we demonstrate that Y. ptb spreads extraintestinally in waves, translocating directly from the gastrointestinal tract into the bloodstream without prior replication, leading to a shared bacterial population in the blood, liver, and spleen within days of infection. While lymphatic spread has been proposed, our findings indicate that the mesenteric lymph nodes act as a restrictive site in wild-type mice, a function that is lost in the absence of TNF signaling. Overall, this work elucidates the complex interplay of host factors shaping Y. ptb population dynamics during infection, quantifying the bottlenecks to intestinal colonization and tissue invasion. These findings enhance our understanding of Y. ptb invasive infection and may inform the development of therapeutics for severe invasive bacterial infections.