Chikungunya virus (CHIKV) is a re-emerging mosquito-borne alphavirus, which causes debilitating arthritis-like symptoms in humans. While determinants of CHIKV host cell entry into mammalian cells are known, their equivalents in mosquito cells remain largely elusive. To identify CHIKV entry factors in Aedes mosquito cells, we engineered a virus encoding the pro-apoptotic Drosophila Reaper gene, which was subsequently used to perform a near-genome wide CRISPR knockout screen. CHIKV-Reaper induced cell death in C6/36 cells upon infection and displayed normal replication kinetics in mammalian cells, while being slightly attenuated in C6/36 cells. Using the C6/36 cell-based CRISPR screening platform, we identified three cell surface proteins and multiple enzymes involved in their biosynthesis pathway. Using gene silencing in Aedes aegypti and Aedes albopictus cells, we confirmed that one of the three proteins, an immunoglobulin-like domain-containing membrane protein, is a CHIKV host factor. In line with these findings, transcomplementation of refractory mammalian cells with one of the host factors rendered cells susceptible to both West African and East Central South African CHIKV lineages. Moreover, transcomplementation rendered cells susceptible to other arthritogenic alphaviruses including Semliki Forest virus (SFV) and Ross River virus (RRV), while the encephalitic alphavirus Venezuelan equine encephalitis virus (VEEV) could not enter transcomplemented cells. Altogether, we identified a receptor for CHIKV in mosquitoes and demonstrate that recombinant pro-apoptotic arboviruses efficiently enable CRISPR knockout screens in insect cells.