The tourists were 140-4, needing a further 183 runs in 23 overs to reach their target of 323, when Dhoni walked out to bat at the home of cricket.
It was a situation that cried out for some belligerent batting from the often aggressive Dhoni, one of the best finishers of a white-ball innings in the modern game.
Yet instead, Dhoni made a sedate 37 off 59 balls with just two fours.
When he eventually holed out off Liam Plunkett with a rare lofted shot, India were effectively beaten at 215-8 with just under four overs remaining.
India were bowled out for 236 off the last ball of the match as England won by 86 runs to level the three-match series at 1-1 ahead of Tuesday's finale at Headingley.
Dhoni's innings may not have been quite as extraordinary as India great Sunil Gavaskar's infamous 'go-slow' against England at Lord's in the inaugural match of the first World Cup in 1975, when the celebrated opener carried his bat for 36 not out in a 60-over match his side lost by a mammoth 202 runs, but it was curious all the same.
England Test paceman Stuart Broad, commentating on Sky Sports, said of Dhoni: "Today he never really quite got going and he had no fluency to his batting — two boundaries in 59 balls, and you're not going to win too many games doing that."
Meanwhile former India off-spinner Harbhajan Singh added: "Today was definitely a different Dhoni we got to see. He normally does take his time, but then once he's in he looks for the boundary. But, today he was short of partners, though he still probably defended too many balls."
But Kohli defended the 37-year-old Dhoni, a veteran of 320 ODIs who effectively won the 2011 World Cup final for India against Sri Lanka in Mumbai off his own bat, by saying: "This comes up again and again when he is not able to play in the normal way he does. It's very unfortunate people just jump to conclusions very quickly."
Kohli added: "When he does well, people call him the best finisher ever and when they don't go well, they all pounce on him. We all have bad days in cricket and today was a bad one for everyone, not just him. Also, you want to take the innings deep; you don't want to just lose by 160-170 runs, and he has the experience, but some days it just doesn't come off. Other people jump to conclusions, but we don't — we totally believe in him."
COMMENTS
Comments are moderated and generally will be posted if they are on-topic and not abusive.
For more information, please see our Comments FAQ