T-cell lymphomas (TCLs) comprise a heterogeneous group of malignancies. Current therapeutic options remain limited, partly given the scarcity of representative preclinical models. To uncover targetable vulnerabilities, we created a collection of TCL patient-derived-tumor-xenografts (PDXs) retaining molecular and histomorphology donor tumor features over serial xeno-grafting while capturing their mechanisms of lymphomagenesis and evolution. Ex-vivo cultures and in-vivo experiments demonstrated remarkable heterogeneity, complex intra-tumor genomic architecture, and stepwise genomic trajectories. The transcriptional representation of primary and PDXs led to a new classification comprising four novel microenvironment-based TCL subtypes. The library identified a unique subset expressing T-cell receptors recognizing Epstein-Barr Virus (EBV) peptides supporting a novel EBV-mediated tumorigenic mechanism. Mechanistically, we uncovered a pro-tumorigenic role of stromal elements and elucidated bidirectional lymphoma-microenvironment interactions. Importantly, PDXs captured individual vulnerabilities, mirrored donor patients clinical responses, and defined effective patient-tailored treatments. This platform represents a public resource for discovering and validating oncogenic drivers and new drugs/combinations.