Hyalinizing clear cell carcinoma (HCCC) is a rare indolent malignant tumor of minor salivary gland origin with EWSR1::ATF1 rearrangement. Pathologically, the tumor cells possess a clear cytoplasm in a background of hyalinized stroma. Generally, the tumor cells are positive for p63 and p40, and negative for s100 and αSMA, suggesting that they differentiate into squamous epithelium and not into myoepithelium. In this study, we performed a detailed histopathological and genomic analysis of six cases of HCCC including two atypical subtypes-a case of high-grade transformation and one with possessing a novel partner gene for EWSR1. We performed a sequential analysis of the primary and recurrent tumor by whole-exome sequencing, RNA sequencing, Sanger sequencing, and fluorescence in situ hybridization (FISH) to investigate the effect of genomic changes on histopathology and clinical prognosis. A fusion gene involving the EWSR1 gene was detected in all cases. Five cases, including the high-grade transformation, harbored a known EWSR1::ATF1 fusion gene; however, one case harbored a novel EWSR1::LARP4 fusion gene. This novel EWSR1::LARP4 fused HCCC has a SOX10 positive staining which is different from the EWSR1::ATF1 fused HCCC. According to whole-exome sequencing and FISH analysis, the Whole-genome doubling and, focal deletion involving CDKN2A, CDKN2B and PTEN were detected in HCCC with high-grade transformation. Conclusively, we identified a novel partner gene for EWSR1, LARP4, in indolent HCCC. Importantly, high-grade transformation and poor prognosis were caused by whole genome doubling and subsequent genomic aberrations.