Species genetic diversity can reflect their adaptability to environmental changes. Coral reefs worldwide are in rapid decline due to climate change and human activities, highlighting the need for conservation intervention. The South China Sea (SCS) is an important biodiversity hotspot, particularly in the Xisha Islands (XS) that contain the majority of coral species in the SCS. However, few studies exist on coral genetic diversity in the SCS. Montipora digitata is the dominant reef-building coral species in the XS. In this study, two mitochondrial DNA fragments and 11 microsatellite markers were employed to investigate the genetic diversity of coral host of M. digitata, and ITS amplicon sequencing was employed to investigate the Symbiodiniaceae community structure. We sampled five wild populations of M. digitata in Hainan Island and the Xisha Islands. Montipora digitata showed low genetic diversity across populations in the SCS. We found significant genetic differentiation between the Sanya (SY) and XS populations but no significant genetic differentiation within XS populations. We identified four Symbiodiniaceae genera, with Cladocopium and Durusdinium being the most common, as well as Gerakladium and Fugacium. The Symbiodiniaceae types of SY and XS are significantly different, C15 is abundant in all populations, while D1a is also abundant in SY. We analyzed the correlation between 16 environmental factors and the genetic diversity of symbionts, genetic diversity of coral host and Symbiodiniaceae community was significantly correlated with sea surface temperature (SST) and other environmental factors. Our study provided a detailed paradigm from the perspective of genetic diversity of how a dominant coral species can be indicative of poor environmental adaptation potential.