The transcription factor Prdm14 is a potent oncogene implicated in the initiation of many cancers. PRDM14 resets and maintains the pluripotent state in normal cells, but the molecular mechanisms through which PRDM14 drives oncogenesis are poorly understood. Here, we interrogated the heterogeneity of Prdm14-expressing cells in a T cell lymphoblastic leukemia/lymphoma mouse model. Using mass cytometry (CyTOF) of bone marrow at a pre-leukemic timepoint, an unexpected abnormal progenitor B cell population was identified. Prdm14-expressing progenitor B cells demonstrated short-term self-renewal and a block in differentiation when transferred to syngeneic hosts. Consistently, aged host mice succumb to a highly penetrant B-LL. Single-cell RNA-seq analyses suggests that the expression signature of these pre-leukemia cells is more consistent with that of B-1 cells than B-2 cells. B-1 cells are a self-renewing population of unconventional B cells established during embryonic development. Overlaying the chromatin binding of transcriptional marks H3K4me1 and H3K4me3 with PRDM14 suggests that PRDM14 initiates cancers through promiscuous DNA binding, activating oncogenic pathways and skewing development towards a self-renewing B-1-like phenotype. Together, our data show that Prdm14 can initiate premature T and B cell cancer programs when expressed in hematopoietic progenitor cells.