Nairo Quintana's Movistar was third at 4 seconds, Alberto Contador's Tinkoff-Saxo fourth at 28 seconds with reigning champion Vincenzo Nibali's Astana fifth at 35 seconds.
The result pulled BMC’s Tejay van Garderen one second closer to Froome and also saw key general classification contender Contador edge closer to the top, with Quintana also moving into the top 10 overall.
The biggest casualty of the time trial was defending champion Nibali, who at 2min 22sec behind Froome after the stage lost valuable time and is in danger of losing contact with the elite group.
While the stage was short, it was strategically placed, coming after eight days of hard, dangerous racing. It was this positioning that left many teams and riders with questions to answer.
The course was also an atypical one, ignoring the usual pancake flat profile seen on stages like the 28km from Vannes to Plumelec in favour of one that was rolling, ending with an uphill pinch.
Lampre-Merida waited for five teams to finish before its time of 33min 03sec was bettered by IAM to the tune of 10 seconds.
Next into the hot seat with a time of 32min 50sec was Nibali's Astana outfit. But despite the position, its ride was not a smooth one after losing two riders early and struggling to hold its shape to the finish.
The lead changed again almost immediately as Movistar shot past the unexpectedly soft time set by Astana, but its 32min 19sec was also nowhere near what would be required to win the stage.
BMC, the pre-race favourite, then took the hotseat as expected but by only by four seconds with Tinkoff-Saxo in third place.
The wait was then on for Froome and Sky, which had a five second advantage at the foot of the final 1.7km, 6.2 per cent climb to the finish in Plumelec.
In danger of losing the fifth man required to record a time, Sky had to slow to wait for Nicolas Roche to hitch back on, and the delay made all the difference for BMC.
"We really can't be too disappointed with that, within a second of BMC, but yes, for everyone's morale it would have been fantastic to get the stage win today," Froome said.
Van Garderen's mood was considerably more chipper than that of Froome, and he praised Australian team-mate Rohan Dennis, who won the Stage 1 inidividual time trial at this Tour, for his part in the victory.
"It feels damn good. From this morning we all had this feeling today was going to be a great day," the American said.
"When we got out on the course, everything just slotted into place, and luckily we had that motor Rohan Dennis out there to give us some long, hard pulls."
Van Garderen has flown somewhat under the radar this Tour, but remains confident of a strong finish to the Tour, and he remains very much in contention.
"This first week couldn't have really gone much better. Sport is all about momentum, once you pick up some steam it just keeps trolling," he said. "We've got momentum on our side now, and we want to keep that going all the way to Paris."
Australia’s Orica-GreenEDGE, the last squad to have won the TTT at the Tour de France two years ago, rode conservatively after starting the stage three riders down owing to the abandons of Simon Gerrans, Daryl Impey and Michael Albasini to first week crashes.
Michael Matthews is also not firing at full capacity with popped ribs from his involvement in the Stage 3 crash that finish Gerrans and Impey's Tours.