Specific recognition of the viral genome is an essential step in the assembly of most viruses, including tailed bacteriophages. In numerous tailed phages, such as SPP1, genome packaging is initiated by recognition and cleavage of a specific sequence pac, by the small (TerS) and large (TerL) terminase subunits. Cleavage at pac occurs only once, initiating a packaging series along a substrate concatemer. The packaging cycle is terminated by a non-specific sequence cleavage determined by the amount of DNA inside the capsid, yielding packaged molecules longer than the phage genome (headful packaging mechanism). It was previously shown that the SPP1 pac region has two sequences where TerS binds (pacR and pacL) flanking the segment where TerL cleaves the SPP1 DNA (pacC). However, the pac specific sequences required to achieve this endonucleolytic cut were not established. Their characterization is essential to understand the underlying mechanism. In this study we used a plasmid minimal system encoding SPP1 pac, TerS and TerL that mimics specific pac recognition and its auto-regulated cleavage in Bacillus subtilis. the SPP1 host. We show that the pacR sequence localized within 35 bp downstream of the pac cut can be extensively degenerated, including its c1 and c2 repeats, and that only disruption of a 5 bp polyadenine tract impairs pac cleavage. This result together with deletion analysis of pacL shows that the specific DNA sequences required for targeting the terminase for pac cleavage are considerably shorter than the large region bound by TerS. Furthermore, extensive degeneration of the 6 bp target sequence within pacC where pac cleavage occurs, reveals that TerL maintains, remarkably, its precise position of cleavage. Studies with SPP1-related phages show conservation of the cut position, irrespectively of sequence variation in pacC, in pacR or changes in pacL-pacC distance. Mechanistically our data are compatible with a model in which TerS interactions with part of the pacL sequence and a poly-A tract in pacR are sufficient to orient very accurately the TerL nuclease to a defined pacC position. They also demonstrate that the resulting precise cut at pacC is independent of the targeted DNA sequence.