Diverse eukaryotic cells crawl through complex environments using distinct modes of migration. To understand the underlying mechanisms and their evolutionary relationships, we must define each mode, and identify its phenotypic and molecular markers. Here, we focus on a widely dispersed migration mode characterized by dynamic, actin-filled pseudopods that we call "α-motility." Mining genomic data revealed a clear trend: only organisms with both WASP and SCAR/WAVE---activators of branched actin assembly---make pseudopods. While SCAR has been shown to drive pseudopod formation, WASP's role in this process is murky. We hypothesize that these genes together represent a genetic signature of α-motility, and are used for pseudopod formation. WASP depletion from human neutrophils confirms that both proteins are involved in explosive actin polymerization, pseudopod formation, and cell migration, and colocalize to dynamic signaling structures. Moreover, retention of WASP together with SCAR correctly predicts α-motility in disease-causing chytrid fungi, which we show crawl at >30 μm/min with actin-filled pseudopods. By focusing on one migration mode in many eukaryotes, we identified a genetic marker of α-motility and evidence for a widely distributed mode of cell crawling with a single evolutionary origin.