ΦGT1 is a lytic podovirus of an alphaproteobacterial Sulfitobacter species, with few closely matching sequences among characterized phages, thus defying a useful description by simple sequence clustering methods. The history of the ΦGT1 core structure module was reconstructed using timetrees, including numerous related prospective prophages, to flesh out the evolutionary lineages spanning from the origin of the ejectosomal podovirus >3.2 Gya to the present genes of ΦGT1 and its closest relatives. A peculiarity of the ΦGT1 structural proteome is that it contains two paralogous tubular tail A (tubeA) proteins. The origin of the dual tubeA arrangement was traced to a recombination between two more ancient podoviral lineages occurring ~0.7 Gya in the alphaproteobacterial order Rhizobiales. Descendants of the ancestral dual A recombinant were tracked forward forming both temperate and lytic phage clusters and exhibiting both vertical transmission with patchy persistence and horizontal transfer with respect to host taxonomy. The two ancestral lineages were traced backward, making junctions with a major metagenomic podoviral family, the LUZ24-like gammaproteobacterial phages, and Myxococcal phage Mx8, and finally joining near the origin of podoviruses with P22. With these most conservative among phage genes, deviations from uncomplicated vertical and nonrecombinant descent are numerous but countable. The use of timetrees allowed conceptualization of the phage’s evolution in the context of a sequence of ancestors spanning the time of life on Earth.