Iflaviruses are non-enveloped single-stranded RNA viruses, which infect various insects including economically important agricultural pollinators honeybees and bumblebees. Studies of the life cycle and pathogenesis of iflaviruses are impeded by the lack of a honeybee cell cultures. Here, we present two crystal structures of an iflavirus Slow Bee Paralysis Virus (SBPV) purified from a natural source, solved at 3.4 Å and 2.6 Å resolutions. We found that the C-terminus of a capsid protein VP3 forms a protruding domain (P-domain) located on the virion surface. The P-domain exhibits a novel fold, which is different from that seen in any other viruses characterized to date. P-domains undergo large movements toward icosahedral five-fold axis, where they are found in a crown-like arrangement. Despite sharing the same quasi T=3 symmetry with known insect picorna-like viruses, SBPV exhibits a unique surface topology and differs in the overall organization of the capsid. Our findings provide structural framework for further investigations of infection mechanisms employed by the agriculturally important class of viral pathogens.