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Comparative genomic studies across the eukaryotic tree have provided valuable insights into eukaryotic evolution, but many key microbial taxa have been overlooked due to their absence from culture collections. Among these taxa are the largely neglected Rhizaria, a supergroup and member of the Stramenopile, Alveolate, Rhizaria (SAR) clade that comprises approximately 60% of all eukaryotic diversity. Although ubiquitous in the environment, the Rhizaria have received limited attention in terms of molecular and cell biology, development, and genetics compared to other lineages due to difficulty establishing and maintaining laboratory cultures. Nonetheless, Rhizarian amoeboid protists offer insights into the evolution of multicellularity, morphological complexity, and mechanisms for spatial differentiation during their often multiphasic lifecycles. Many Rhizarian amoebae exhibit a network of reticulopodia, specialized pseudopodia that form a branched morphology resembling neuronal arbors. Despite the striking morphological similarities, the cell biology and shared components between Rhizarian amoebae and metazoan neurons remain poorly understood.This study presents the first comprehensive genomic description and cytoskeletal investigation of Filoreta ramosa, a Rhizarian multinucleate (syncytial) amoeba isolate. Using fluorescence imaging and drug perturbations, we reveal the remarkable similarity of Filoreta's cytoskeleton to that of neurons, suggesting an ancient conserved mechanism driving this morphology. The elaborate cytoskeletal architecture enables rapid organelle transport and dynamic reorganization in response to the environment. Notably, the interphase microtubule array in Filoreta syncytia organizes longitudinally, facilitating bidirectional transport and displaying potential for parallel and antiparallel bundling through non-centrosomal nucleation. Furthermore, Filoreta demonstrates versatility by forming lamellipodia and filopodia, indicating a diverse repertoire of actin and actin-associated cytoskeletal proteins. Genome analysis uncovers cytoskeletal and signaling proteins that further support Filoreta's neuron-like behavior during the development of its complex arborized network and environmental sensing. The findings shed light on the cell biology and mechanisms underlying the intriguing convergence between Rhizaria and metazoan neurons. Additionally, we present a robust cultivation method for free-living amoeboid protists, expanding the available models for future investigations of non-model amoeboid organisms at the molecular, cellular, developmental, and genetic levels. This multiphasic analysis sets the stage for further research into the evolutionary and functional aspects of Rhizaria, offering valuable insights into eukaryotic cytoskeletal evolution.