The young Foxes, who overcame Norwich City 4-3 at the end of January, welcomed the Saints to Seagrave knowing a victory would enable them to climb above the south coast outfit in the standings.
It was the visitors who went close first as Luke Pearce's powered shot was smothered by the outrushing Foxes goalkeeper Arlo Doherty before losing Diamond Edwards to injury early on.
City, meanwhile, took the lead on 22 minutes as Oli Ewing, who starred for the Development Squad last week, raced into the box curled it past Saints shot-stopper Matt Hall and into the bottom left corner.
Chris Popov and Tawanda Maswanhise had opportunities for Leicester's youngsters in the second half, too, but they were both denied by the impressive Hall for Southampton.
Tyler Dibbling, promoted from the Saints' Under-15s side, earned a free-kick for the visitors with 10 minutes, but Kami Doyle saw his effort crash back off the crossbar before being cleared by City.
The result sees the young Foxes climb above Southampton to 12th in the U18 Premier League South Division standings, on eight points, ahead of hosting Crystal Palace on Saturday (12pm GMT kick-off).
City: Doherty; Lindsay, Kutshitnza, Obi, Cook; Popov, Butterfill (Cartwright 64'), Ewing, Cover; Maswanhise, K. Pennant.
Subs not used: Weeks, Lewis, Javid.
Goal: Ewing 22'.
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