Early-life gut colonization is a major ecological bottleneck for host-associated microbes because the neonatal intestine remains transiently oxygenated before becoming fully anaerobic. Although Bacteroides fragilis is a strict anaerobe, it displays strong fitness during neonatal colonization, suggesting the existence of stage-specific adaptive mechanisms. Here, we identify a species-specific glycosphingolipid, alpha-galactosylceramide (BfaGC), as a key determinant of this early-life fitness. Using genome-wide transposon sequencing during vertical transmission in gnotobiotic mice, we found that neonatal colonization depends on oxidative respiration-related pathways and on agcT, the gene required for BfaGC biosynthesis. Deletion of agcT selectively impaired neonatal colonization, whereas heterologous expression of agcT conferred a competitive advantage in early life to a non-BfaGC-producing Bacteroides strain. Mechanistically, BfaGC was induced by oxygen exposure and promoted aerotolerance by stabilizing membrane bioenergetics, preserving proton motive force, and supporting oxygen-dependent respiration. In addition to enhancing microbial fitness, neonatal BfaGC production was associated with host immune modulation, linking bacterial adaptation to developmental host-microbe interactions. Together, these findings identify BfaGC as a stage-specific colonization factor that enables B. fragilis to overcome transient oxygen stress in the neonatal gut and provide a molecular framework for host-microbiome co-adaptation in early life.