Alexis Sanchez's superb free-kick opened the scoring for an Arsenal side featuring 10 changes from the weekend.
But Southampton hit back soon after as Dusan Tadic scored a penalty given for a foul on debutant Sadio Mane.
A stunning strike from Nathaniel Clyne gave the Saints a deserved lead, which they protected in a lively second half.
Ronald Koeman's side continue to make a mockery of the pre-season suggestions that they were en route to mediocrity following the summer exodus of their manager and five key players.
In contrast to the changes made by opposite number Arsene Wenger, Koeman made five alterations to his starting XI and was rewarded with a coherent display consistent with the quick counter-attacking style they have showcased this campaign.
They had to show resolve to come from behind after Sanchez had put Arsenal ahead by curling a superb free-kick over the wall and into the top corner from 25 yards.
It took them six minutes to respond as Mane, playing his first game since obtaining a work permit, drew a trip out of Tomas Rosicky in the box and Tadic side-footed his penalty down the middle to equalise.
Clyne's goal to give them the lead and ultimately the win was as brilliant as it was unexpected. The defender picked up the ball following a cleared corner, took a touch and smashed a shot that swerved past Arsenal's debutant keeper David Ospina and into the roof of the net.
Arsenal strove for an equaliser in the second half but they were unable to break down the visitors, who could easily have added to their lead but for some wayward shooting.
None of the players Wenger drafted in did much to stake a claim for a first-team place.
Rosicky covered ground but provided relatively little, Lukas Podolski and Joel Campbell were largely anonymous, while Abou Diaby, making his first start since March 2013, was understandably off the pace.
That the midfielder managed over an hour after such a lengthy period out with yet another injury is the most positive development Wenger can take away from the evening.
Arsenal manager Arsene Wenger:
"It's disappointing because we had a good start and we made two unneeded errors on the two goals - and big ones.
"We lacked a bit of experience at the back, but overall they did well. We gave a lot and it's frustrating not to be able to score in the second half.
"When you look at the amount of possession we had, we have to give credit to Southampton, they played well and were well organised.
"They abused a bit the fouls in the middle of the park, but they are a good side and they played well tonight. Overall it is frustrating because we gave a lot."
Southampton manager Ronald Koeman:
"I'm very proud, because winning away against Arsenal, that means a lot.
"Everybody spoke about the changes of the Arsenal team. I think they made some changes but they took it very seriously.
"I think the game was on a very high level, with high tempo, and I enjoyed it.
"We tried to press and tried to play attractive, offensive, and that's not easy, because they have a great team, great players."
Sanchez has now scored four goals for Arsenal since his summer move from Barcelona
Tadic scored from the penalty spot to claim his first goal as a Southampton player
Clyne's fourth goal for Southampton was an absolute screamer from over 35 yards
Arsenal boss Arsene Wenger made 10 changes from the team that beat Aston Villa 3-0 on Saturday.
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