Organohalide-respiring bacteria (OHRB) are key contributors to global halogen cycling and mitigation of anthropogenic halogenated pollutants, yet their persistence is challenged by slow growth and restricted metabolic capacity. The mechanisms supporting long-term functional stability remain unclear. As a key OHRB, Dehalococcoides faces similar constraints, including declining abundance and loss or divergence of functional genes in bioaugmentation. Here we demonstrate that strain-level microdiversity within Dehalococcoides supports the resilience of community-scale dehalogenation. In AEDhc, a reconstructed consortium derived from eight Dehalococcoides-containing enrichment cultures, sequencing of a Dehalococcoides-specific marker gene revealed 30 distinct Dehalococcoides phylotypes coexisting within the community. Despite fluctuations in phylotype abundance over successive transfers, AEDhc consistently debrominated tetra- and pentabrominated diphenyl ethers (0.39 ± 0.06 - 0.45 ± 0.05 μM Br^–/d), producing no detectable accumulation of intermediates. Proteomics analyses revealed that among 71 putative reductive dehalogenase (RDase) genes identified in metagenomic analysis, expression was consistently dominated by PcbA1-like and TceA-like RDases across transfers. These findings demonstrated that Dehalococcoides phylotypes can coexist and fluctuate dynamically even under constant cultivation conditions, with genetic variation serving as a reservoir of metabolic potential. Such microdiversity enhances functional stability and ecological resilience, highlighting the need to consider strain-level heterogeneity in bioremediation strategies.