The tournament's second-seeds beat fellow Australian pair Jason Kubler and Johns Peers 7-6 (7-4) 7-5.
In the first set of the Atlanta Open final, neither side managed to break the other with Kyrgios and Kokkinakis edging the tie-break 7-4.
The second set followed a similar pattern with both pairs serving strongly before The Special Ks claimed a decisive break in what would be the final game of the match.
They were forced to abandon plans to play at Wimbledon in July but managed to reunite in Atlanta despite Kyrgios being unable to play singles due to a lingering injury.
The Atlanta double champions will now go their separate ways before the US Open begins in late August.
Kyrgios is heading to Washington to play in the Citi Open and will also be teaming up with American Jack Sock in the men's doubles.
Kokkinakis, meanwhile, is bound for Mexico where he'll play in the Los Cabos Open singles as the tournament's seventh-seed.
The Special Ks are expected to unite to play men's doubles at the US Open with a third title together now in their sights.
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