During embryonic development, cell-fate specification gives rise to dedicated lineages that underlie tissue formation. In olfactores, which comprise tunicates and vertebrates, the cardiopharyngeal field is formed by multipotent progenitors of both cardiac and branchiomeric muscles. The ascidianCionais a powerful model to study cardiopharyngeal fate specification with cellular resolution, as only two bilateral pairs of multipotent cardiopharyngeal progenitors give rise to the heart and to the pharyngeal muscles (also known as atrial siphon muscles, ASM). These progenitors are multilineage primed, in as much as they express a combination of early ASM- and heart-specific transcripts that become restricted to their corresponding precursors, following oriented and asymmetric divisions. Here, we identify the primed gene ring finger 149 related (Rnf149-r), which later becomes restricted to the heart progenitors, but appears to regulate pharyngeal muscle fate specification in the cardiopharyngeal lineage. CRISPR/Cas9-mediated loss ofRnf149-rfunction impairs atrial siphon muscle morphogenesis, and downregulatesTbx1/10andEbf, two key determinants of pharyngeal muscle fate, while upregulating heart-specific gene expression. These phenotypes are reminiscent of the loss of FGF/MAPK signaling in the cardiopharyngeal lineage, and an integrated analysis of lineage-specific bulk RNA-seq profiling of loss-of-function perturbations has identified a significant overlap between candidate FGF/MAPK andRnf149-rtarget genes. However, functional interaction assays suggest thatRnf149-rdoes not directly modulate the activity of the FGF/MAPK/Ets1/2 pathway. Instead, we propose thatRnf149-racts both in parallel to the FGF/MAPK signaling on shared targets, as well as on FGF/MAPK-independent targets through (a) separate pathway(s).