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Weaning is a critical stage in the growth and development of piglets, often inducing stress reactions. This study aims to investigate the effects of <i>Parabacteroides distasonis</i> (PBd) derived from Ningxiang pigs on growth performance, intestinal apoptosis, oxidative damage, and inflammation in ETEC-challenged weaned piglets. A total of 22 Duroc × Landrace × Yorkshire (DLY) piglets, 24 days old with similar body weights, were randomly divided into three groups: Control (<i>n</i> = 7), ETEC (<i>n</i> = 7), and PBd + ETEC (<i>n</i> = 8). The results show that, compared to the Control group, ETEC challenge led to decreased growth performance, reduced villus height in the duodenum and jejunum, increased crypt depth in the duodenum, a decreased villus-height-to-crypt-depth ratio, increased expression of apoptosis-related genes (<i>Caspase-8</i> and <i>Caspase-9</i>), increased expression of oxidative damage-related genes (<i>Nrf2</i>, <i>GSH-PX</i>, <i>mTOR</i>, and <i>Beclin1</i>), increased expression of inflammation-related genes (<i>Myd88</i>, <i>P65</i>, <i>TNF-α</i>, and <i>IL-6</i>), and reduced the contents of SCFAs in the colonic chyme (acetate, propionate, butyrate, valerate, and total SCFAs). Compared to the ETEC group, the PBd + ETEC group alleviated the reduction in growth performance, mitigated intestinal morphological damage, and reduced the expression of the aforementioned apoptosis, oxidative damage, and inflammation-related genes with the increase in SCFAs. In conclusion, PBd derived from Ningxiang pigs effectively reduces ETEC-induced intestinal damage in weaned piglets, improves intestinal health, and increases the content of SCFAs in the colonic chyme, thereby enhancing growth performance.