Early-life gut microbiome development influences infant growth, immune maturation and infection risk, yet we still lack a unified ecological understanding of how the first colonisers at birth shape later succession—and how these rules generalise across global populations. We integrate longitudinal, genome-resolved metagenomics from high-income settings and low- and middle-income cohorts to reveal conserved assembly programmes and pinpoint microbial traits that underpin stability and pathogen resistance. In a UK neonatal cohort, initial colonisation begins in one of several distinct pioneer community states, each dominated by a single species. Dominance by Bifidobacteria—particularly Bifidobacterium breve and Bifidobacterium longum—is associated with stable trajectories and durable colonisation resistance, consistent with priority effects and supported by germ-free mouse experiments; by contrast, alternative pioneer states are linked to more stochastic assembly and persistent pathogen burden. Extending beyond birth, we generated a globally harmonised, genome-resolved map of microbiome assembly by integrating infants from LMICs spanning sub-Saharan Africa and South Asia. Despite marked taxonomic differences between sites, microbiomes converge on a feeding-synchronised, stage-resolved succession from milk/mucin specialists to weaning-associated plant-glycan metabolisers, while key metabolic and host-relevant functions persist through replacement by functionally complementary taxa. Finally, a global genome catalogue of Bifidobacterium infantis and Bifidobacterium longum resolves species-level divergence and reveals strong biogeographic strain structure and substrate adaptations, informing stage- and geography-aware interventions that restore missing functions and strengthen pathogen resistance in early life.