E3 ligases constitute an important component of proteostasis machinery which plays a critical role in the survival of malaria parasite through post-translational modifications of its protein-substrates. In contrast to humans, parasite E3 ligases have not been extensively studied. Here, we characterize a unique Plasmodium E3 ligase that has both RING and HECT-like features with zinc-coordinating domains. Plasmodium encodes a single RING-between-RING (RBR) E3 ligase that has evolutionarily diverged from human and other intracellular parasites. This RBR-E3 ligase is expressed throughout the erythrocytic phase of P. falciparum lifecycle. Immunoprecipitation experiments showed that Pf RBR-E3 ligase catalyzes K6, K11, K48 and K63 mediated polyubiquitination hinting towards its diverse biological roles (DNA repair, proteasomal degradation, mitochondrial quality control). We observed that Pf RBR-E3 ligase interacts with UBCH5 and UBC13 family of E2-conjugating enzymes. Through mutational analysis, we identified residues in RING1 and RING2 domains that are critical for ubiquitination activity and protein stability of Pf RBR-E3 ligase. Our experiments showed that Pf RBR-E3 ligase participates in maintenance of organellar homeostasis and exhibits differences in immunofluorescence profile upon exposure of parasite to different genotoxic (MMS) and proteotoxic (MG132, FCCP and artemisinin derivative) stress. Our study opens up avenues for exploring the client substrates of Pf RBR-E3 ligase and using this knowledge to design substrate-specific protein degradation based alternative intervention strategies for malaria.