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Simple Summary: Mannheimia haemolytica (M. haemolytica) is a significant bacterial pathogen that causes substantial economic losses to the livestock industry by infecting ruminants. In our previous study, we successfully isolated and identified a strain of M. haemolytica from Hainan Black goats. However, the pathogenicity of this strain and the molecular mechanism underlying the interaction between M. haemolytica and animals have not been investigated. In this study, we constructed a M. haemolytica infection model in mice to analyze the histopathology of the bacterial infection and explore the immune mechanisms employed by the murine spleen to resist M. haemolytica infection. (1) Background: Mannheimia haemolytica (M. haemolytica) is an opportunistic pathogen and is mainly associated with respiratory diseases in cattle, sheep, and goats. (2) Methods: In this study, a mouse infection model was established using a M. haemolytica strain isolated from goats. Histopathological observations were conducted on various organs of the mice, and bacterial load determination and RNA-seq analysis were specifically performed on the spleens of the mice. (3) Results: The findings of this study suggest that chemokines, potentially present in the spleen of mice following a M. haemolytica challenge, may induce the migration of leukocytes to the spleen and suppress the release of pro-inflammatory factors through a negative feedback regulation mechanism. Additionally, an interesting observation was made regarding the potential of hematopoietic stem/progenitor cells congregating in the spleen to differentiate into immune cells, which could potentially collaborate with leukocytes in their efforts to counteract M. haemolytica invasion. (4) Conclusions: This study revealed the immune regulation mechanism induced by M. haemolytica in the mouse spleen, providing valuable insights into host–pathogen interactions and offering a theoretical basis for the prevention, control, and treatment of mannheimiosis. [ABSTRACT FROM AUTHOR]