Class I PI3K, encoded by the PIK3CA gene, generates PI(3,4,5)P3 at the plasma membrane following growth factor receptor activation and is mutated and hyperactive in many cancers. PI(3,4,5)P3 is degraded by the tumour suppressor PTEN to PI(4,5)P2 terminating PI3K signaling. Alternatively, inositol polyphosphate 5-phosphatases degrade PI(3,4,5)P3 to PI(3,4)P2 and INPP4A/B degrades PI(3,4)P2 to form PI(3)P and thereby inhibits PI3K-dependent AKT signaling in many cancers. INPP4A is known to localise to early endosomes where it degrades PI(3,4)P2 to form PI(3)P and regulates endocytosis and Akt signalling. Recently, INPP4B was identified a tumor suppressor in breast and ovarian cancer via regulation of PI3K/Akt signalling at the plasma membrane. Triple negative breast cancers are associated with increased PI(3,4)P2/Akt signaling and poor long-term outcome. Paradoxically recent studies have shown in colon cancer and acute myeloid leukemia increased INPP4B expression has been reported and may function as an oncogene, independent of Akt signalling. How these paradoxical opposing INPP4B actions relate to PI3K pathway regulation is unclear. We reported PIK3CA-mutant ER+ breast cancers show increased INPP4B mRNA and protein expression. INPP4B increased the proliferation and tumor growth of PIK3CA-mutant ER+ breast cancer cells, despite reducing AKT signaling. Using an "omics" approach with integrated proteomics, transcriptomics and imaging, INPP4B was localized to late endosomes via an interaction with Rab7, which increased endosomal PI3Kα-dependent PI(3,4)P2 to PI(3)P conversion, late endosome/lysosome number and cargo trafficking to late endosomes. The increased number of late endosomes enhanced GSK3β lysosomal degradation and thereby activated Wnt/β-catenin signaling. Inhibition of Wnt signaling, or depletion of the PI(3)P-effector Hrs, reduced INPP4B-mediated cell proliferation and tumor growth. This data predicts INPP4B facilitates the cross talk between class I PI3Kα with oncogenic Wnt signaling on late endosomes in ER+ breast cancer by PI(3,4)P2 to PI(3)P conversion.