Now, ahead of the Champions Trophy that opens in England and Wales this week, Dhoni has been burdened with another task -- defending the alleged sins of his pay-masters.
Indian cricket was thrown into chaos last month when three players, including recent Test bowler Shanthakumaran Sreesanth, were arrested for alleged spot-fixing during the glitzy Indian Premier League.
Further trouble mounted Sunday for the country's powerful cricket chief, Narayanswamy Srinivasan, who stepped aside from his post while a police investigation over his son-in-law Gurunath Meiyappan's links to illegal bookmakers remained ongoing.
Meiyappan was accredited as 'team owner' of the IPL franchise Chennai Super Kings, owned by Srinivasan's business venture India Cements, leading to a revolt in the Indian board against their boss.
Dhoni shares a special bond with Srinivasan, not only as captain of India and the Chennai Super Kings, but also as a vice-president of India Cements, an appointment made earlier this year.
As he plots India's strategy ahead of their Champions Trophy opener against South Africa in Cardiff on Thursday, Dhoni has also been busy fending off questions about the scandal back home.
The unruffled 31-year-old has done a good job of keeping cool till now, but it remains to be seen how long he can maintain his composure.
"When the right time comes, I will answer it," Dhoni said when bombarded with IPL-related queries at his opening media conference in England last week.
"As of now, I want to keep our side away from everything."
Sourav Ganguly, who took over as India's captain soon after the match-fixing episode in 2000 that led to the downfall of Mohammad Azharuddin and the late South Africa captain Hansie Cronje, sympathised with Dhoni.
"Dhoni is in a tough position at the moment," Ganguly was quoted as saying in the Indian media. "I can sympathize with him as everyone wants an explanation from him.
"But it is not his fault that he was picked up by Chennai Super Kings. It is not his fault that Gurunath (Meiyappan) is involved in betting."
Dhoni will know that he and his team can restore Indian cricket's damaged reputation by doing well on the field, starting with the eight-nation Champions Trophy.
And he has the credentials to undertake a revival.
Last year, an extraordinary career that began as a railway ticket inspector in his home state of Jharkhand, saw Dhoni hailed by Forbes magazine as the world's richest cricketer with annual earnings of $26.5 million.
Taking over as captain in 2007 when senior players declined to take part in the inaugural World Twenty20 in South Africa, Dhoni engineered one of India's most remarkable runs in the sport.
Under him, India won the World Twenty20 in 2007, rose to number one in the Test rankings in 2009 and lifted the 50-over World Cup in 2011, with Dhoni hitting he winning six against Sri Lanka in the Mumbai final.
But two humiliating 4-0 Test whitewashes in England and Australia, followed by a rare home series defeat against England last year, led to calls for Dhoni's removal from the side altogether.
Dhoni not only retained the captaincy -- only due to Srinivasan's intervention -- but also hit back by leading India in a 4-0 rout of Australia in a Test series at home earlier this year.
He will now have to show similar dexterity to pull Indian cricket out of a hole again.