Lipophagy—the lysosome-dependent degradation of lipid droplets (LDs)—is essential for energy homeostasis and lipid turnover. It proceeds via two main pathways: canonical macroautophagy and direct lysosome–LD interactions. However, unlike protein- or organelle-selective autophagy, lipophagy has remained difficult to monitor due to the lipid-based nature of LDs and the lack of specific reporters. Here, we present LD-AUTag1, a novel small-molecule fluorescent probe that enables real-time quantification of lipophagy in live cells and organisms. The probe emits green fluorescence for neutral LDs and red fluorescence upon delivery to lysosomes, reporting lipolysosome formation as a direct readout of lipophagy. LD-AUTag1 specifically detects lipophagy induced by serum starvation, but not lipolysis triggered by amino acid deprivation. Its performance was validated using high-throughput flow cytometry and confocal microscopy in cell models and extended to whole-organism imaging in Dictyostelium and zebrafish. Importantly, LD-AUTag1 revealed key features of lysosomal dysfunction such as lipolysosome accumulation caused drastic enhancement of red signals and aberrant morphology. In live blood cells and immortalized lymphocytes, the probe enabled sensitive detection of lysosomal storage disorders (LSDs), distinguishing affected samples from healthy and heterozygous controls. It also revealed hallmark lipid accumulations and aberrant lysosomal morphology undetectable by conventional dyes. Together, these results establish LD-AUTag1 as a powerful, generalizable tool for monitoring lipophagy dynamics and lysosomal integrity. This probe offers broad potential for disease diagnostics and fundamental lipid biology research.