An increasing number of genomic studies are showing that genetic introgression between closely related species is surprisingly common across the tree of life, thus making the description of biodiversity and understanding the process of speciation complex and challenging. The adaptive radiation of cichlid fishes in Lake Malawi, with hybrid origins and recent cases of introgression, provides an important model system to study the evolutionary implications of introgression. However, many potential sources of introgression into the radiation have not yet been investigated. Here we use whole genome data from 239 cichlid species from Lake Malawi and a comprehensive dataset of 76 species from surrounding African river and lake systems to discover and map previously unknown introgression events involving the Malawi cichlid radiation. Using genome-wide excess allele sharing (ABBA BABA statistics) and window-based analyses, we found that three independent riverine cichlid lineages are significantly closer to the Malawi radiation than to its sister group, suggesting historical genetic exchange between these lineages and the Malawi radiation. Across Malawi species, we found low variability in the levels of excess allele sharing with non-Malawi species, suggesting that introgressed haplotypes are distributed relatively uniformly across the radiation and that most hybrid-derived polymorphism was acquired and sorted before the formation of the contemporary Malawi cichlid radiation. Our results point towards several previously unknown contributors to the Malawi hybrid swarm, suggesting that the history of one of the largest vertebrate radiations was even more complex than previously thought.