India were theoretically the away side at Edgbaston but were roared on by a crowd that was weighed heavily in their favour.
After the game was reduced to 20 overs a side following almost six hours of rain, Dhoni's side looked set to send them home disappointed.
From 66 for five, Virat Kohli (43) and Ravindra Jadeja (33 not out) hauled India to the relative respectability of 129 for seven, but England still appeared favourites.
At that stage a washout and a share of the trophy seemed India's best prospect.
But Dhoni refused to let his players hope for rain and instead gave them the confidence to secure outright success as England fell short on 124 for eight.
"Before going on I said 'let's get rid of the feeling that this is a 50-over game'," he said. "It was a 20-over game and we have seen at the IPL and in Twenty20s that 130 can be a very difficult target to achieve.
"Also I said nobody could look to the left side of the pitch where the rain was coming from.
"I said 'God is not coming to save us, if you want to win the trophy we have to fight it out'.
"We are the No 1-ranked side, let's make it show. Let's make them fight for 130 runs and not look for outside help."
Dhoni, as magnanimous a leader as India have had, even found time to query the very format that had brought his side success.
"I think it is a bit unfair in the ICC Champions Trophy that we had to play a 20-over game to find a winner of the 50-over format," he said. "Still, they [the ICC] needed a result. This means a lot because we are playing here against some of the best sides in the world and to beat England in a 130-run game is very difficult."
Dhoni was left to offer individual praise for man of the tournament and top run-scorer Shikhar Dhawan and leading wicket-taker Ravindra Jadeja for their efforts in the competition.
"Shikhar is a slightly different character. He's a fun-loving guy but he backs himself to play big strokes. That has helped him in this tournament and he'll gain a lot from the way he has played over here.
"And Jadeja is someone who keeps it very simple. He looks to hit the right area and the ball does the talking."
Meanwhile Alastair Cook, Dhoni's opposite number, has precious little time to dwell on the defeat – a disappointment he agrees is his worst as captain.
The opening batsman will now fine-tune England's preparations for their next major assignment – the first of back-to-back Ashes series, starting at Trent Bridge on July 10.
England are on Monday due to name their squad to face Cook's own county Essex in a four-day warm-up match – a selection which will be mighty close to the one eventually confirmed for that first Test against Australia in Nottingham.
Cook and colleagues must therefore switch their attention quickly, but the England Test and ODI captain accepts it will take a short time to come to terms with events in Birmingham.
"It will take a couple of days. It's a tough pill to swallow at the moment. We had high hopes...of achieving something special," Cook said.
Come what may in the remainder of this season, the left-hander anticipates the squad which came so close in the Champions Trophy will be back – with the likely addition of Kevin Pietersen – to try again down under in the next World Cup.
"I think the majority of the squad will be pretty similar...in 2015, you'd hope. It's obviously not a great place to be in the dressing room at the moment.
"But when you start looking back at what we've done well – which areas we can work on – obviously, Ashley and I will have a look at that."
Cook did not try to hide his dismay after Ravi Bopara – with 30 runs and three wickets for 20 – had helped to get England so close.
At 110 for four, they still had 16 balls left with two set batsmen at the crease.
But it was not to be.
"Clearly from there you would back yourself to win more times than you would lose. But it shows how quickly games can change in Twenty20 when you lose a couple of wickets. We just couldn't quite get over the line."
Cook felt England were not solely responsible for their own downfall, and was particularly aggrieved by third umpire Bruce Oxenford's decision to give Ian Bell out stumped.
Television replays were far from conclusive, and he said: "I thought it was a poor decision. It loomed pretty clear that he was in."
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