Viruses infecting freshwater bacteria are generally unexplored. Flavobacteria are ubiquitous freshwater bacteria that have a major role in biochemical cycles and contribute to water quality in lakes and rivers. We have explored boreal freshwaters for phages infecting highly abundant species of Flavobacterium. Genomic analysis revealed high variability in phage genome sizes (up to 380 kbp) and long reads of unknown sequence. From 25 isolates, four were detected to be large i.e. jumbo phages (genome size over 200 kbp). Also a novel phage type was isolated – a tailless, membrane containing phage, named FLiP, possessing a circular ssDNA genome. From the 9174 nt genome 16 open reading frames (ORFs) were predicted, majority of them having no significant sequence similarity to the database. The structure of FLiP virion was solved using electron cryomicroscopy and a notable similarity to a marine dsDNA phage PM2 was seen. FLiP is the first characterized ssDNA phage to possess an inner lipid membrane. Among bacterial viruses it is also the first to link different genome types to a similar structure. Hence our data suggests that boreal freshwaters can serve as an excellent source for exploring virus diversity and evolution.