Long noncoding RNAs (lncRNAs) are a large and diverse class of genes in eukaryotic genomes that contribute to a variety of regulatory processes. Functionally characterized lncRNAs play critical roles in plants, ranging from regulating flowering to controlling lateral root formation. However, findings from the past decade have revealed that thousands of lncRNAs are present in plant transcriptomes, and characterization has lagged far behind identification. In this setting, distinguishing function from noise is challenging. However, the plant community has been at the forefront of discovery in lncRNA biology, providing many functional and mechanistic insights that have increased our understanding of this gene class. In this review, we examine the key discoveries and insights made in plant lncRNA biology over the past two and a half decades. We describe how discoveries made in the pregenomics era have informed efforts to identify and functionally characterize lncRNAs in the subsequent decades. We provide an overview of the functional archetypes into which characterized plant lncRNAs fit and speculate on new avenues of research that may uncover yet more archetypes. Finally, this review discusses the challenges facing the field and some exciting new molecular and computational approaches that may help inform lncRNA comparative and functional analyses.