Post-transcriptional processing and modification of mRNA is essential for eukaryotic gene expression and is regulated by a complex network of RNA-binding proteins (RBPs). Bacterial pathogens use specialised secretion systems to inject “effector” proteins into the host cell that hijack cellular processes to subvert host immunity. In this study, we describe the effector protein LegC4 from Legionella pneumophila as an RBP that degrades host mRNA during infection. Cryo-EM structural analysis of an inactive mutant of LegC4 (LegC4H60A) in complex with single-stranded RNA was performed to isolate its N-terminal RNA-binding domain (RBD) at 6-angstrom. This revealed a six-stranded anti-parallel beta-sheet platform and adjacent alpha-helix which mediated RNA contacts as well as the molecular basis for the putative ribonuclease activity of LegC4. Importantly, the LegC4 RBD lacked homology to known RBDs (e.g., RRM or KH domains) suggesting that it represents a non-canonical protein fold that can interact with single-stranded RNA. This work is the first description of a secreted bacterial effector that functions as an RBP and provides insights into alternative structural domains that mediate RNA-interactions.