Aaron Ramsey sent Steve Thompson racing towards the by-line and when he hooked the ball back into the danger area Parry was waiting to smash in his tenth goal of the season.
The only change to the Bluebirds starting line-up was Ramsey in for the injured Darcy Blake.
The Saints threatened straight from the kick-off when a Stern John backheel went to Mario Licka, but his side-footer skimmed the outside of the home post.
But it was the Bluebirds who went ahead against the run of play when Parry blasted the ball high into the net from close range.
Midway through the half Jhon Viafara met a deep cross, but could not direct his shot on target and City went straight back on attack, only for Joe Ledley's shot to be saved by the legs of Saints keeper Richard Wright.
A mistake by Roger Johnson caused problems for the Bluebirds defence in the 36th minute and the visitors had the ball in the net, only for the referee's assistant to flag for offside.
Seven minutes after the restart John missed an open goal when he failed to connect following a Southampton corner. The Bluebirds were looking very ragged at the back and it only seemed a matter of time before the Saints equalised.
Bradley Wright-Phillips was brought on after an hour as Nigel Pearson's side continued to take the game to City.
The Bluebirds countered ten minutes later when Trevor Sinclair replaced Whittingham, but still it was the visitors who looked more dangerous going forward.
Johnson and Glenn Loovens had to be at their best as the visitors threatened the home goal, but despite seeing more of the ball, they were unable to carve out any clear openings and the Bluebirds held out for the three points.