The modular architecture of multi-domain enzymes is a key source of functional diversity. GH18 chitinases exemplify this, possessing a variety of auxiliary domains that have been postulated to underpin their role as essential global nutrient cyclers. However, there is no evolutionary framework that accounts for vast the assortment of domain compositions observed across the protein family. Here, we map the sequence space of nearly 40,000 bacterial chitinases, integrating phylogenetics with a quantitative analysis of domain promiscuity to decode their evolutionary history. We reveal that diversification follows distinct trajectories: enzymes necessary for environmental chitin scavenging evolve via high modular plasticity and structural elaboration of the catalytic core, whereas sequences required for specialized, essential developmental roles fix their domain architecture to fulfill lineage-specific physiological roles. By resolving how domain accretion co-evolves with catalytic scaffolds, this work provides a framework for understanding how multi-domain enzymes adapt to complex environments.