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(1) Background: <i>Mannheimia haemolytica</i> (<i>M. haemolytica</i>) 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 <i>M. haemolytica</i> 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 <i>M. haemolytica</i> 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 <i>M. haemolytica</i> invasion. (4) Conclusions: This study revealed the immune regulation mechanism induced by <i>M. haemolytica</i> in the mouse spleen, providing valuable insights into host–pathogen interactions and offering a theoretical basis for the prevention, control, and treatment of mannheimiosis.