Microbial communities thriving in hypersaline brines of solar salterns are highly resistant and resilient to environmental changes, and salinity is a major factor that deterministically influences community structure. Here, we demonstrate that this resilience occurs even after rapid osmotic shocks caused by a threefold change in salinity (a reduction from 34 to 12% salts) leading to massive amounts of archaeal cell lysis. Specifically, our temporal metagenomic datasets identified two co-occurring ecotypes within the most dominant archaeal population of the brines Haloquadratum walsbyi that exhibited different salt concentration preferences. The dominant ecotype was generally more abundant and occurred in high-salt conditions (34%); the low abundance ecotype always co-occurred but was enriched at salinities around 20% or lower and carried unique gene content related to solute transport and gene regulation. Despite their apparent distinct ecological preferences, the ecotypes did not outcompete each other presumably due to weak functional differentiation between them. Further, the osmotic shock selected for a temporal increase in taxonomic and functional diversity at both the Hqr. walsbyi population and whole-community levels supporting the specialization-disturbance hypothesis, that is, the expectation that disturbance favors generalists. Altogether, our results provide new insights into how intraspecies diversity is maintained in light of substantial gene-content differences and major environmental perturbations.