It was perhaps a bad performance long in the making for Sharma, though, who despite not having a record to write home about, has remained a permanent fixture of Indian sides virtually since 2007.
The 25-year-old's Test record is a disappointing 144 wickets at 51 matches at an average of a well-above the generally accepted average for a top-class bowler of 38.
His one-day international record is then poor also with 96 wickets in 68 matches at a relatively high average of over 31 and a high economy rate of 5.70.
It has been somewhat baffling why Sharma has continually been selected to play with India as the No. 1 quick bowler despite not having the record to back it up with, and now this could be the chance for the selectors to make a statement and send him back to work on improving his game.
India were cruising to victory when Sharma was brought back into the attack to bowl the 48th over.
Four sixes and 30 runs from Australian allrounder James Faulkner later and the match had swung drastically in the tourists' favour.
Sharma, already under pressure to retain his place for the remaining four matches of the series, cut a disconsolate figure on the field after Australia's incredible comeback win.
Indian fans were immediately calling for Sharma's head, while hanging their own in shame - but Dhoni said the towering quick was hurting more than anyone.
"When you are disappointed, it's always better to give the individual a bit of time to think by himself," Dhoni said after the match.
"The ideal time (to talk to Sharma) is after going back to the hotel. That's when you have a chat.
"When you are representing your country in front of 30,000 people, if you bowl a bad over, no one wants to bowl a bad over, the individual is more disappointed than anyone, in the stadium or in the team."
Prior to the last of his eight overs, Sharma had enjoyed his best game of the series - taking the crucial wicket of Aaron Finch while owning figures of 1-33 from seven overs.
"We are talking about one over or two overs," Dhoni said.
"The rest... no one is talking about.
"When he gave us the wicket, that was the time we really needed the wicket.
"Overall, you have to see everything. Not one or two bad overs.
"If a batsman plays one bad shot, you can't judge a batsman. If someone is going through a bad period, that's when the team backs him."
Dhoni wouldn't discuss whether Sharma would, as expected, be dropped for the remainder of the series - leaving that decision to the selectors.
"If it is a selection matter, I will discuss it with the selectors and not at a press conference," he said.
"If you base everything on one or two games, the whole team will have to be changed.
"It would be unfair if you want to throw away bowlers from the playing XI after one or two games.
"It's very important to persist with them and give them experience."
ISHANT SHARMA'S HORROR 48th OVER WHICH JAMES FAULKNER HIT FOR 30 RUNS
Ball one: Full and wide, Faulkner hits it sweetly over cover and it races to the boundary for four.
Ball two: Shorter, Faulkner picks up the length early and swings hard over cow corner for six. Flies about 25 rows back and the ball takes several minutes to return from the crowd.
Ball three: A short-length ball is picked beautifully and sent straight back over the bowler's head for another monster six.
Ball four: Another shorter delivery is smacked to deep square leg. A four seems certain but the ball is saved on the boundary. Two runs.
Ball five: Another short ball is hooked high and long by Faulkner into the crowd. Six more runs.
Ball six: Sharma drops short once more and Faulkner is all over it. A sweetly-timed pull sails into the stands for six more to bring up Faulkner's 50.