Long non-coding RNAs (lncRNAs) are receiving increasing attention as biomarkers for cancer diagnosis and therapy. Although there are many computational methods to identify cancer lncRNAs, they do not comprehensively integrate multi-omics features for predictions or systematically evaluate the contribution of each omics to the multifaceted landscape of cancer lncRNAs. In this study, an algorithm, POCALI, is developed to identify cancer lncRNAs by integrating 44 omics features across six categories. The contributions of different omics are explored to identifying cancer lncRNAs and, more specifically, how each feature contributes to a single prediction. The model is evaluated and benchmarked POCALI with existing methods. Finally, the cancer phenotype and genomics characteristics of the predicted novel cancer lncRNAs are validated. POCALI identifies secondary structure and gene expression-related features as strong predictors of cancer lncRNAs, and epigenomic features as moderate predictors. POCALI performed better than other methods, especially in terms of sensitivity, and predicted more candidates. Novel POCALI-predicted cancer lncRNAs have strong relationships with cancer phenotypes, similar to known cancer lncRNAs. Overall, this study facilitates the identification of previously undetected cancer lncRNAs and the comprehensive exploration of the multifaceted feature contributions to cancer lncRNA prediction.