Despite the intestinal microbiota’s critical role in enhancing host defense against diseases, the ecological mechanisms driving shifts in intestinal microbiota during infection and their interplay with host immunity remain poorly characterized. Here, we examined the dynamics and interactions between the intestinal microbiota and host immunity in Litopenaeus vannamei following Vibrio parahaemolyticus infection. Our results demonstrated a marked rise in bacterial diversity within shrimp intestines post-infection, along with a transition to a more heterogeneous community structure and heightened complexity in bacterial interactions. The relative abundances of the dominant intestinal bacterial taxa (e.g., Candidatus Bacilloplasma, Demequina , Tamlana , and Motilimonas ) either increased in infected shrimp intestines. On the contrary, V. parahaemolyticus infection imposed significant selective pressure on Candidatus Bacilloplasma, the bacterial genus with the highest relative abundance, leading to a significant decline in the intestinal abundance of this bacterium in infected shrimp. More precisely, at 72 h, 120 h, and 168 h post-infection, the relative abundances of Candidatus Bacilloplasma in control shrimp intestines were 31.34%, 34.52%, and 49.01%, respectively, while they dropped to 19.99%, 21.43%, and 12.19% in infected shrimp intestines. We further observed surge in microbial diversity and evenness, as well as the enhanced intricacy of bacterial networks, likely stemming from ecological niche opportunities created by the pronounced decline in Candidatus Bacilloplasma. Additionally, the infection by V . parahaemolyticus evidently altered the predicted function of the intestinal bacterial community in shrimp. For example, aminoacyl-tRNA biosynthesis, ribosome, and purine metabolism were significantly downregulated, while 2-Oxocarboxylic acid metabolism was significantly upregulated at 120 h and 168 h post-infection. Notably, deterministic processes, particularly host immune selection, became prominent in shaping the shrimp intestinal microbiota post-infection, leading to a sharp reduction in Candidatus Bacilloplasma prevalence. This research deepens our understanding of the complex interplay between intestinal microbiota and pathogenic infection in shrimp, highlighting the essential role of native intestinal bacteria in sustaining microbial homeostasis and host health.