Dynamic intracellular lipid trafficking is needed to maintain the various membrane compositions of cells and organelles. GRAMD1b is a recently discovered lipid transfer protein (LTP) crucial to governing cholesterol transport from the plasma membrane (PM) to the endoplasmic reticulum (ER), a process triggered by phosphatidylserine (PS). Despite this, the mechanisms mediating PS delivery to the PM during this process are unclear. We found GRAMD1b is in the close proximity with the PS transporters ORP5/8. ORP5/8 are known to function at ER-associated membrane contact sites (MCS), exchanging PS and phosphatidylinositides (PIPs) between the ER and other organelles, including the PM, mitochondria, and lipid droplets. Cholesterol loading initiates the recruitment of ORP5/8 to the ER-PM junction. Using CRISPR, we generated ORP5/8 double knockout (DKO) Hela cells. In the absence of ORP5/8, GRAMD1b failed to reach the ER-PM junction after cholesterol loading. The phenotype can be rescued by overexpressing either ORP5 or ORP8 in the ORP5/8 DKO cells. PIP2 is known to be important for the recruitment ORP5/8 to the PM, and cholesterol loading also increases PIP2 level on the PM. Significantly, the acute depletion of PIP2 prevents ORP5/8 and GRAMD1b recruitment to the plasma membrane under these conditions, demonstrating PIP2 has a crucial role in regulating PM-ER cholesterol transport. These findings add new pieces to the puzzle of intracellular cholesterol trafficking.