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Simple Summary: Cylapocoris is a genus of the cylapine tribe Fulviini distributed in the Neotropics, with most species being recorded from Central America. By the descriptions of five new species and redescriptions of six species, we provide a robust amount of morphological data, including the novel study of female genitalia, offering an updated diagnosis and description of the genus. This paper also elucidates the phylogenetic position of the genus and the interrelationships of the species within it as well as confirming the monophyly of Cylapocoris. This paper provides descriptions of five new species of the Neotropical genus Cylapocoris Carvalho, 1954 (C. bimaculatus n. sp., C. brooksi n. sp., C. carvalhoi n. sp., C. scutellatus n. sp., and C. simplexoides n. sp.). Cylapocoris and Cylapocoroides Carvalho, 1989 are redescribed and rediagnosed. Illustrations of male genitalia, scanning electron micrographs of selected structures of certain taxa, and an identification key to species are provided. Female genitalia are described and illustrated for the first time for Cylapocoris in nine out of 19 known species. A cladistic analysis of the genus, based on 62 morphological characters, is presented as a contribution to the understanding of relationships within Cylapocoris and its relationships with other groups of Cylapinae. The analysis comprises 16 ingroup species and 15 outgroup taxa. Both equal and implied weighting parsimony analyses were used in the phylogenetic reconstruction. We confirm the monophyly of Cylapocoris and its sister-group relationship with Cylapocoroides. Additionally, we identify subgroupings within Cylapocoris. Intertribal relationships within Cylapinae are briefly discussed. [ABSTRACT FROM AUTHOR]