Retrograde communication from axonal targets to neuronal cell bodies is critical for both development and function of the nervous system. Much progress has been made in recent years linking long-distance, retrograde signaling to a signaling endosome, yet the mechanisms governing the trafficking and signaling of these endosomes remain mainly uncharacterized. Here we report that in mouse sympathetic neurons the target-derived NGF-TrkA signaling endosome, upon arrival at the cell body, induces the expression and recruitment of a novel effector protein known as Coronin-1. In the absence of Coronin-1, the NGF-TrkA signaling endosome fuses to lysosomes 6–10 fold faster than when Coronin-1 is intact. We also define a novel Coronin-1-dependent trafficking event where signaling endosomes recycle and re-internalize upon arrival at the cell body. Beyond influencing endosomal trafficking, Coronin-1 is also required for several NGF-TrkA dependent-signaling events including calcium release, calcineurin activation, and CREB phosphorylation. These results establish Coronin-1 as an essential component of a novel feedback loop mediating NGF-TrkA endosome stability, recycling, and signaling as a critical mechanism governing developmental competition for survival.