Hepatocellular carcinoma (HCC) has high relapse and low 5-year survival rates. Single-cell profiling in relapsed HCC may aid in the design of effective anticancer therapies, including immunotherapies. We profiled the transcriptomes of ∼17,000 cells from 18 primary or early-relapse HCC cases. Early-relapse tumors have reduced levels of regulatory T cells, increased dendritic cells (DCs), and increased infiltrated CD8+ T cells, compared with primary tumors, in two independent cohorts. Remarkably, CD8+ T cells in recurrent tumors overexpressed KLRB1 (CD161) and displayed an innate-like low cytotoxic state, with low clonal expansion, unlike the classical exhausted state observed in primary HCC. The enrichment of these cells was associated with a worse prognosis. Differential gene expression and interaction analyses revealed potential immune evasion mechanisms in recurrent tumor cells that dampen DC antigen presentation and recruit innate-like CD8+ T cells. Our comprehensive picture of the HCC ecosystem provides deeper insights into immune evasion mechanisms associated with tumor relapse. Display omitted •ScRNA-seq reveals a distinct immune ecosystem in early-relapse HCC•Decreased Tregs, increased DCs, and CD8+ T cells were observed in early-relapse HCC•CD8+ T cells have an innate-like, low cytotoxic, and low clonal expansion phenotype•Recurrent malignant cells mediate the compromised antitumor immune response Single-cell analysis of primary and relapsed hepatocellular carcinoma tumors from patients reveal innate-like CD8+ T cells with low cytotoxicity and clonal expansion in the latter that may explain the compromised antitumor immunity and poor prognosis associated with liver cancer.