Ovarian cancer remains one of the most lethal gynaecological malignancies, largely due to late diagnosis and limited targets. Although long noncoding RNAs (lncRNAs) are increasingly recognised as key regulators of cancer biology; their cell-type-specific roles during ovarian tumour emergence and treatment remain poorly understood. Here, we developed a pseudo-longitudinal framework integrating lncRNA discovery, patient-derived transcriptomic profiling and RNA-targeting CRISPR screening to investigate lncRNA functions in ovarian cancer. Deep bulk RNA-seq from the tissues-of-origin was used for de novo transcriptome assembly and lncRNA discovery, generating an adnexal metatranscriptome containing 23,861 high-confidence lncRNAs. This resource, together with annotated transcripts were used as custom reference to interrogate transcriptional changes across a curated meta-cohort of single-cell RNA-seq datasets spanning normal ovary (young and mature), normal fallopian tube, benign ovarian lesions, and treatment-naïve and chemoresistant ovarian tumours. Samples were ordered by clinical and pathological staging into cross-sectional trajectories of tumour emergence and chemoresistance. Co-expression analysis using an ovarian cancer marker panel prioritised 675 lncRNAs strongly associated with malignancy, approximately 75% of which were previously unannotated. Of the annotated lncRNAs, nearly 20% have already been linked to ovarian cancer. We also identified a subset of lncRNAs able to discriminate early-stage tumours from normal tissue, highlighting their potential as biomarkers for early detection. Cell-type annotation uncovered stage-dependent remodelling of the tumour microenvironment, with expansion of epithelial cells across all stages, loss of mesenchymal cells during disease onset, and an increase in immune cells during tumour emergence that declined after treatment. Analysis of each major population independently, identified distinct lncRNA trajectories characteristic of disease progression and resistance. Prioritised candidates are currently being functionally validated using CRISPR-Cas13d proliferation and treatment-survival screens. Together, this study provides the most comprehensive pseudo-longitudinal atlas of lncRNA dynamics across ovarian cancer emergence and treatment response, establishing a valuable resource of the discovery of biomarkers and therapeutic targets.