Bovill and Allison will be joint heads of the unit, taking over from Tom Tagholm, who left in March to pursue commercial projects.
At Fallon, they created the multi-award-winning "cake" and "mean green" campaigns for Skoda, as well as the Cadbury "Spots v Stripes" work.
The duo were promoted to creative partners and joined the management board at Fallon earlier this year.
Channel 4’s chief marketing and communications officer, Dan Brooke, said: "Chris and John are wunderkinds of their generation in advertising. They’ll be to TV like ships are to water and lead our hugely talented team to wonderful new creative lands."
4Creative produces all through-the-line advertising for Channel 4, Film4, More4 and E4, including digital campaigns, brand identity work, publishing, radio, product design and ambient activity.
It recently created the acclaimed "meet the superhumans" and "thanks for the warm-up" on- and off-air campaigns to promote the broadcaster’s coverage of the Paralympic Games.