Telomerase reverse transcriptase (TERT) promoter mutations occur frequently in cancer, have been associated with increasedTERTexpression and cell proliferation, and could potentially influence therapeutic regimens for melanoma. As the role ofTERTexpression in malignant melanoma and the non-canonical functions of TERT remain understudied, we aimed to extend the current knowledge on the impact ofTERTpromoter mutations and expression alterations in tumor progression by analyzing several highly annotated melanoma cohorts. Using multivariate models, we found no consistent association forTERTpromoter mutations orTERTexpression with the survival rate in melanoma cohorts under immune checkpoint inhibition. However, the presence of CD4+ T cells increased withTERTexpression and correlated with the expression of exhaustion markers. While the frequency of promoter mutations did not change with Breslow thickness,TERTexpression was increased in metastases arising from thinner primaries. As single-cell RNA-sequencing (RNA-seq) showed thatTERTexpression was associated with genes involved in cell migration and dynamics of the extracellular matrix, this suggests a role ofTERTduring invasion and metastasis. Co-regulated genes found in several bulk tumors and single-cell RNA-seq cohorts also indicated non-canonical functions ofTERTrelated to mitochondrial DNA stability and nuclear DNA repair. This pattern was also evident in glioblastoma and across other entities. Hence, our study adds to the role ofTERTexpression in cancer metastasis and potentially also immune resistance.