Formins are an evolutionarily old family of cytoskeletal regulators whose roles include microfilament capping, actin nucleation, and modulation of microtubule dynamics. Plant class I formins typically exhibit a unique domain organization, with most of them being transmembrane proteins with possible cell wall-binding motifs exposed to the extracytoplasmic space. Although such transmembrane formins are traditionally considered mainly as plasmalemma-localized proteins, they could also, at least temporarily, reside in endomembranes. Some of them decorate the plasmodesmata. We are currently developing techniques to use a photoswitchable fluorochrome for examining the effects of formin mutations on intercellular transport. Moreover, the main housekeeping Arabisopsis thaliana class I formin, AtFH1, relocates between the plasmalemma and several endomembrane compartments during cell division and differentiation in root tissues, with transient tonoplast localization at the transition/elongation zone border. However, it is unclear whether the tonoplast-localized AtFH1 performs any biologically relevant function or whether is merely briefly occurs at the tonoplast en route towards vacuolar degradation. We shall present observations suggesting that both possibilities are mutually compatible: while mutational loss of AtFH1 affects tonoplast organization, the formin also enters the vacuole lumen. Another Class I formin, AtFH5, also enters the vacuole via an autophagic pathway under certain conditions and contributes to specific stress resistance. We propose a model where class I formins may serve as “active cargoes” of membrane trafficking, i.e. membrane-embedded proteins that modulate the fate of membrane compartments they reside on. This work has been supported by the Czech Science Foundation grant 22-33471S.