Dysregulated iron metabolism is a hallmark of cancer. Moreover, increased trapping of iron in protoporphyrin IX, to generate bioavailable heme-iron, is considered a tumor dependency, especially in KRAS mutated pancreatic and lung cancers. While the mechanisms orchestrating the rise in labile iron levels in proliferating cells have been extensively studied, the factors triggering heme biosynthesis activation in tumors remain poorly understood. Our research elucidates the essential role of the plasma membrane transporter Feline Leukemia Virus subgroup C Receptor 1a (FLVCR1a) in driving heme biosynthesis in proliferating cells: depletion of this transporter leads to decreased ALAS1-dependent heme biosynthesis, hindering the development of a glycolytic profile in KRAS-mutated tumor cells and consequently reducing tumor initiation, growth, and dissemination. We propose that enhanced expression of FLVCR1a in tumor cells is part of the rewiring of iron metabolism and serves as one of the triggering events harnessed by cells to transition from a non-proliferative to a proliferative state. The recent revelation that this transporter, previously thought to export heme, can import choline and/or ethanolamine opens up new avenues, suggesting that oncogene-induced modulation of lipid metabolism could be the initial trigger for stimulation of heme biosynthesis, in order to initiate and sustain proliferation.