While canonical 3'end modifications of mRNAs or tRNAs are well established, recent technological advances in RNA analysis have given us a glimpse of how widespread other types of distinctive 3'end modifications appear to be. Next to alternative nuclear or cytoplasmic polyadenylation mechanisms, evidence accumulated for a variety of 3'end mono-nucleotide and oligo-nucleotide additions of primarily adenosines or uracils on a variety of RNA species. Enzymes responsible for such non-templated additions are non-canonical RNA nucleotidyltransferases, which possess surprising flexibility in RNA substrate selection and enzymatic activity. We will highlight recent findings supporting the view that RNA nucleotidyltransferase activity, RNA target selection and sub-compartimentalization are spatially, temporally and physiologically regulated by dedicated co-factors. Along with the diversification of non-coding RNA classes, the evolutionary conservation of these multifaceted RNA modifiers underscores the prevalence and importance of diverse 3'end formation mechanisms.