Ph-like acute lymphoblastic leukemia is a high-risk subtype of leukemia that is driven by a range of genetic aberrations and chromosomal arrangements. In this subtype, chimeric fusion proteins are significant drivers of constitutive kinase activation. We report a novel fusion between CD74 and PDGFRB in a pediatric patient with B-ALL. The patient had high residual blasts following induction chemotherapy, consistent with induction failure. Given the indication of a PDGFRB lesion, the patient proceeded to receive dasatinib in conjunction with consolidation therapy as a curative bridge to a CAR T cell infusion. Sequence analysis of the CD74::PDGFRB fusion revealed an unusual structure with no clear in-frame transcript arising from exon 1 of CD74. Molecular dissection exposed a non-canonical in-frame ATG start codon within PDGFRB that drives expression of a truncated PDGFRB protein. Structural modelling revealed that the juxtamembrane domain in the full-length PDGFRB receptor acts as an autoinhibitory loop, this interaction is disrupted in the truncated PDGFRB protein allowing constitutive auto-activation of the kinase. Consistent with this, we show that unlike full-length PDGFRB, expression of CD74::PDGFRB is sufficient to drive downstream signaling and cell transformation in B cell models. This study highlights a new mechanism of kinase activation in Ph-like ALL, wherein the aberrant expression of a ‘loose’ kinase domain is sufficient to drive auto-activation and leukemic transformation. This encourages a closer inspection of putative leukemia drivers which may be overlooked following out-of-frame sequence predictions.