Genetic transduction is a major evolutionary force that drives microbial speciation. All bacteriophage-mediated gene transfer is known to occur by one of two well-described mechanisms: generalized and specialized transduction. Herein we report that the temperate phages of Staphylococcus aureus engage in lateral transduction, which we propose to be the most powerful and potentially most impactful mode of phage transduction described to date. Contrary to the established dogma, we found that numerous staphylococcal prophages excise late in their lytic program, so that DNA packaging initiates in situ and proceeds for up to seven or more successive capsid headfuls. Large metameric spans (up to several hundred kb) of the bacterial chromosome are packaged and horizontally transferred at frequencies that are unprecedented for known mechanisms of host gene transfer. While in situ packaging should be catastrophic for phage viability, bidirectional replication precedes DNA packaging and redundancy of the viral genome supports both co-lateral transduction and normal phage reproduction. These results suggest that certain regions of the bacterial chromosome can be considered as hypermobile platforms (of gene transfer): an unconventional take on the genre of mobile genetic elements, defined by genomic coordinates rather than by the DNA elements themselves. In summary, our results show that phage-mediated gene transfer can occur on a scale that is many orders of magnitude greater than previously appreciated, and will lead to a shift in our perception of the impact that phages have on pathogen evolution.