Regulation of pre-mRNA splicing and polyadenylation plays a profound role in neurons by diversifying the proteome and modulating gene expression in response to physiological cues. Although most of the pre-mRNA processing is thought to occur in the nucleus, numerous splicing regulators are also found in neurites. Here, we show that U1-70K/SNRNP70, a component of the major spliceosome, localizes in RNA-associated granules in zebrafish axons. We identify the extra-nuclear SNRNP70 as an important regulator of motor axonal growth, nerve-dependent acetylcholine receptor (AChR) clustering, and neuromuscular synaptogenesis. This cytoplasmic pool has a protective role for a limited number of transcripts regulating their abundance and trafficking inside axons. Moreover, non-nuclear SNRNP70 regulates splice variants of transcripts such as agrin , thereby controlling synapse formation. Our results point to an unexpected, yet essential, function of non-nuclear SNRNP70 in axonal development, indicating a role of spliceosome proteins in cytoplasmic RNA metabolism during neuronal connectivity. [Display omitted] • Spliceosome protein SNRNP70 localizes within axonal RNA granules • SNRNP70 is required in motor neurons for axonal growth and synaptogenesis • Strictly cytoplasmic SNRNP70 can drive key aspects of motor connectivity • Cytoplasmic SNRNP70 modulates the local transcriptional landscape mRNA splicing factors are unexpectedly found in neurites, where their functions are poorly understood. Nikolaou et al. show that U1 spliceosome protein SNRNP70 associates with mRNAs in motor axons and regulates neuronal connectivity. At the molecular level, it modulates local transcriptome composition and mRNA trafficking. [ABSTRACT FROM AUTHOR]