Marie-Antoinette Katoto left defending champions England with a mountain to climb as France came from behind to snatch a priceless Euro 2025 qualifier victory at St James' Park.
Beth Mead had given the Lionesses a 30th-minute lead in head coach Sarina Wiegman's 50th game at the helm, but Elisa De Almeida levelled before the break to set the stage for Paris St Germain striker Katoto to secure a 2-1 win in front of a crowd of 42,561.
The defeat leaves England in third place in Group A3 behind the French and Sweden, who beat the Republic of Ireland 3-0 in Dublin, and knowing that anything less that a win in the reverse fixture in St-Etienne on Tuesday night could scupper any lingering hopes of finishing top.
The top two sides in each group will qualify for next summer’s tournament, with the other two teams facing play-off matches.
A battle between the sides ranked second and third in the world by FIFA was always likely to be tight, but ultimately it was the French who came out on top in a game of fine margins as England suffered their first European Championship qualifying defeat in 24 years.
Wiegman was able to deploy the Leah Williamson-Millie Bright central defensive partnership for the first time since February last year on a night when keeper Mary Earps won her 50th cap.
But Earps' landmark evening lasted less than eight minutes when, having earlier undergone lengthy treatment on the pitch after scuffing a first-minute clearance, she limped off to be replaced by Hannah Hampton.
After an even start, French keeper Pauline Peyraud-Magnin could only look on as Lauren Hemp made the most of Russo's foraging to cross to the near post, where Ella Toone steered her first-time shot just wide of the far upright.
England fail to clear their lines... ❌
— ITV Football (@itvfootball) May 31, 2024
...and France take the lead with a second set piece goal ⚽️ pic.twitter.com/qzGFBX43Vb
Russo fired over from a narrow angle on the turn as the Lionesses continued to press, and they took the lead on the half-hour mark when Mead slotted home from close range after Georgia Stanway had collided with Selma Bacha as the pair attempted to get to Hemp's cross.
The game was far from over, however, and Hampton was relieved to get two hands to Maelle Lakrar's goal-bound header from a 34th-minute Bacha corner to preserve her side's advantage.
However, France were level four minutes before the break when defender De Almeida sent a looping volley over Hampton from Kenza Dali's corner after skipper Wendie Renard created the space with a nudge on Hemp to quieten the partisan home crowd.
Mead might have restored England's lead deep into stoppage time after Russo and Bronze had broken at pace, but her curling effort was brilliantly tipped away by the keeper.
With Keira Walsh and Stanway starting to make their presence felt in a midfield battle which had been shaded by Sakina Karchaoui and Sandie Toletti before the break, the Lionesses once again established a head of steam after the restart.
However, they were fortunate to escape when Cascarino turned Walsh and worked her way into the penalty area before stabbing a 54th-minute shot just wide.
The hosts were having to remain patient as the French defended deep and in numbers, and they were caught by a 68th-minute sucker punch when, having failed to deal fully with Bacha's corner, Katoto pounced to dispatch the ball past Hampton after it had been headed back into the box.
Stanway sent a dipping long-range effort over 14 minutes from time and substitute Chloe Kelly went even closer at the death, but there was no way back.
