Urea has been shown to be important as a nitrogen (N) nutrient for coral holobionts, but the mechanism underpinning urea utilization by symbiotic algae remains unclear. In this study, we investigated the molecular pathways underlying urea utilization in the Symbiodiniaceae family and the responses of these pathways to different N-nutrient conditions and heat stress. Genome screening revealed that two urea hydrolysis systems, urease (URE) and urea amidolyase (UAL), were present in Symbiodiniaceae, positioning this lineage as one of the few non-green algae that possess UAL. Furthermore, our data reveal an interesting evolutionary trajectory of UAL. While subunit DUR2 occurs in thirteen symbiodiniacean genomes sequenced to date, only three symbiodiniaceans possess the complete UAL system (DUR1 with DUR2). In the phylogenetic tree of UAL sequences, Symbiodiniaceae clustered more closely with coral symbiotic bacteria than with other eukaryotes, suggesting horizontal gene transfer from bacteria to Symbiodiniaceae. Furthermore, ex-hospiteCladocopium goreaui exhibited better growth and achieved higher maximum specific growth rates when urea was provided as the sole nitrogen source, compared to ammonium. Notably, when experimenting on the Cladocopium-dominating Pocillopora damicornis holobiont using 15N isotope tracer, we found that under heat stress conditions, the in-hospite Symbiodiniaceae significantly increased urea uptake but decreased NO3- and NH4+ uptake. Omics analyses suggest that responses to different nitrogen, light, and temperature conditions were more likely mediated by UAL. This study reveals two distinct urea utilization systems in the coral ecosystem and their differential responses to warming, highlighting the importance of urea as N-nutrient when facing global warming.