Autophagy cargos include not only soluble cytosolic materials but also bulky organelles, such as ER and mitochondria. In budding yeast, two proteins that contain the PX domain and the BAR domain, Atg20 and Atg24 (also known as Snx42 and Snx4, respectively) are required for organelle autophagy and contribute to general autophagy in a way that can be masked by compensatory mechanisms. It remains unclear why these proteins are important for organelle autophagy. Here, we show that in a distantly related fungal organism, the fission yeast Schizosaccharomyces pombe, autophagy of ER and mitochondria is induced by nitrogen starvation and is promoted by three Atg20- and Atg24-family proteins - Atg20, Atg24 and SPBC1711.11 (named here as Atg24b). These proteins localize at the pre-autophagosomal structure, or phagophore assembly site (PAS), during starvation. S. pombe Atg24 forms a homo-oligomer and acts redundantly with Atg20 and Atg24b, and the latter two proteins can form a hetero-oligomer. The organelle autophagy defect caused by the loss of these proteins is associated with a reduction of autophagosome size and a decrease in Atg8 accumulation at the PAS. These results provide new insights into the autophagic function of Atg20- and Atg24-family proteins.