Former world champion and three-time Olympian Katinka Hosszu (Hungrary), who has battled with the New Zealander for much of the series, pushed through from fourth to second forcing Bowles back to third.
It was an impressive win for Ingram over Hosszu, who is leading the way as the top-ranked woman in the overall series and is chasing the $100,000 bonus.
Matamata's Matthew Stanley had a demanding night, finishing ninth in the 1500m freestyle in 15:01.19 and then backing up with eighth place in the 200m freestyle in 1:47.72.
In other swims, Mitchell Donaldson (North Shore) was 18th in the heats of the 200m individual medley in 2:01.20 and Taranaki's Dylan Dunlop-Barrett was 27th in 2:03.88.
The circuit moves to Singapore this weekend for the final round.
Results from day two of the World Cup swimming meet in Tokyo overnight (NZT):
1500m freestyle: Michael Klueh (USA) 14:38.64, 1; Pal Joensen (PAL) 14:44.83, 2; Ayatsugu Hirai (JPN) 14:45.60, 3. Also: Matthew Stanley (NZL) 15:01.19, 9.
200m freestyle: Darian Townsend (RSA) 1:43.31, 1; Robert Hurley (AUS) 1:43.93, 2; Tomasso D'Orsogna (AUS) 1:44.49, 3. Also Stanley 1:47.72, 9.
100m breaststroke: Glenn Snyders (NZL) 57.98, 1; Akihiro Yamaguchi (JPN) 58.22, 2; Kouichirou Okazaki (JPN) 58.67, 3.
400m freestyle: Melissa Ingram (NZL) 4:05.22, 1; Katinka Hosszu (HUN) 4:05.33, 2; Alanna Bowles (AUS) 4:07.34, 3.