Local Ca2+ elevations boosting phagocytosis are generated in part by the store-operated Ca2+ entry (SOCE) sensor STIM1, which recruits ER cisternae to phagosomes and opens phagosomal Ca2+ channels at ER-phagosome junctions. However, residual ER-phagosome contacts and periphagosomal Ca2+ hotspots remain in Stim1-/- cells. Here, we tested whether junctate, a molecule that targets STIM1 to ER-plasma membrane contacts upon Ca2+-store depletion, could cooperate with STIM1 to recruit ER cisternae to phagosomes. Junctate expression in Stim1-/- and Stim1-/-/; Stim2-/- phagocytic fibroblasts increased phagocytosis and promoted periphagosomal Ca2+ elevations, yet without completely restoring global SOCE. These periphagosomal Ca2+ hotspots were abrogated by the InsP3R specific blocker xestospongin C, revealing that the junctate-mediated Ca2+ ions originate predominantly from Ca2+ stores. Accordingly, junctate elongated ER-phagosome junctions in Stim1-/- cells. Thus, junctate mediates an alternative mechanism for generating localized Ca2+ elevations within cells, promoting Ca2+ release from internal stores recruited to phagosomes, thereby boosting phagocytosis.