And the Scotland international proved the manager right as Wigan finally ended their nightmare run of results.
With ex-England stars David James and Sol Campbell in excellent form for the visitors, it looked like the Latics would have to be content to settle for a point.
But McCulloch, Wigan's longest serving player, popped up to smash in the second-half winner, bagging his fourth of the season to end that dismal record of nine successive defeats, eight of them in the Premiership.
Both sides were looking to get back to winning ways - the Latics desperate to get clear of the relegation zone, and Pompey eager to maintain their push for European qualification.
For Wigan that last taste of success came way back at West Ham in early December, while Portsmouth started the game still to register a Premiership win in 2007.
Paul Jewell still had major injury problems with Leighton Baines and Emile Heskey the latest additions to the casualty list. But there was a debut for £2million striker Julius Aghahowa after just two training sessions with the squad, and Wigan's other newcomer Caleb Folan was making his first appearance at the JJB stadium.
Harry Redknapp had Noe Pamarot back after a groin injury to take over from Djimi Traore, ruled out with an ankle problem. Kanu and Benjani were the front two with Andy Cole on the bench.
Despite their run of results, Wigan made a confident start with new boys Aghahowa and Folan making an early impression.
Folan brought the best out of James with a powerful header from a Ryan Taylor corner and McCulloch burst into the box to fire just wide.
The Latics put together another good attack with David Unsworth's excellent pass flicked on by Aghahowa but Folan's header lacked the power to trouble James.
A defensive slip could have proved disastrous for Pompey but Folan was a fraction slow in reacting to the chance, and James was able to smother the shot.
With the mist rolling in, Wigan keeper Chris Kirkland was twice in action dealing with shots from Kanu and Rudolphe Douala, and Emmerson Boyce came to the rescue getting his boot to the ball to steer it away from the oncoming Benjani.
At the other end, Campbell saved Pompey's bacon with a terrific tackle on Folan, and other opportunities went begging when both Unsworth and the lively Folan failed to find the target.
James again showed his international class after Taylor and Aghahowa combined to set up the strike for Denny Laadzaat. The Dutch star smashed in the volley but James responded with an excellent save.
The Latics threatened again as Taylor went racing clear but defender Pamarot tracked him all the way before finally getting in the tackle to deny him the shot.
But the goal Wigan had been threatening finally arrived when Unsworth's ball was knocked down by Folan and McCulloch raced on to the loose ball to smash it past James.
It visibly lifted the Latics and they almost grabbed a second when Taylor hammered one wide. But they had to survive a nail-biting four minutes of stoppage time before the points were in the bag.