In the Duleep Trophy finals, Dhoni was picked over international cricketer Deep Dasgupta to represent East Zone. He scored a fighting half-century in the second innings in a losing cause. Dhoni's talent was discovered via the BCCI's small-town talent-spotting initiative TRDW. Dhoni was discovered by TRDO Prakash Poddar, captain of Bengal in the 1960s, when he saw Dhoni play for Jharkhand at a match in Jamshedpur in 2003, and sent a report to the National Cricket Academy.

Dhoni studied at DAV Jawahar Vidya Mandir, Shyamali, Ranchi, Jharkhand where he initially excelled in badminton and football and was selected at district and club level in these Sports. Dhoni was a goalkeeper for his football team and was sent to play cricket for a local cricket club by his football coach. Though he had not played cricket, Dhoni impressed with his wicket-keeping skills and became the regular wicketkeeper at the Commando cricket club (1995–1998). Based on his performance at club cricket, he was picked for the 1997/98 season Vinoo Mankad Trophy Under-16 Championship and he performed well. Dhoni focused on cricket after his 10th standard. Dhoni was a Travelling Ticket Examiner (TTE) at Kharagpur railway station from 2001 to 2003, under South Eastern Railway in Midnapore (W), a district in West Bengal. His colleagues remember him as a very honest, straightforward employee of the Indian Railways. But he also had a mischievous side to his personality. Once, while staying at the railway quarters, Dhoni and a couple of his friends covered themselves in white bedsheets and walked around in the complex late in the night. The night guards were fooled into believing that there were ghosts moving around in the complex. The story made big news on the next day.

In 1998, Dhoni was selected by Deval Sahay to play for the Central Coal Fields Limited (CCL) team. Till 1998 Dhoni, who was in class 12th in school, had played only school cricket and club cricket and no professional cricket. One of the famous episodes, when Dhoni used to play for CCL, was when Deval Sahay used to gift him Rs 50 for each six that he hit in Sheesh Mahal tournament cricket matches. Playing for CCL, he got a chance to bat up the order. He grabbed the opportunity and scored centuries and helped CCL move to the A division. Deval Sahay impressed by his hard-hitting shots and dedication, used his contacts in Bihar Cricket Association to push for his selection in the Bihar team. Deval Sahay, an ex Bihar Cricket Association Vice-President, was the Ranchi District Cricket President at that time and was instrumental in pushing Dhoni to the big stage of Ranchi team, junior Bihar cricket team and eventually senior Bihar Ranji Team for the 1999–2000 season. Within 1 year, Dhoni moved from playing in CCL to the Bihar Ranji team. Dhoni was included in the Bihar U-19 squad for the 1998–99 season and scored 176 runs in 5 matches (7 innings) as the team finished fourth in the group of six and did not make it to the quarter-finals. Dhoni was not picked for the East Zone U-19 squad (CK Nayudu Trophy) or Rest of India squad (MA Chidambaram Trophy and Vinoo Mankad Trophy). Bihar U-19 cricket team advanced to the finals of the 1999–2000 Cooch Behar Trophy, where Dhoni made 84 to help Bihar post a total of 357. Bihar's efforts were dwarfed by Punjab U-19s' 839 with Dhoni's Future national squad teammate Yuvraj Singh making 358. Dhoni's contribution in the tournament included 488 runs (9 matches, 12 innings), 5 fifties, 17 catches and 7 stumpings. Dhoni made it to the East Zone U-19 squad for the CK Nayudu trophy but scored only 97 runs in four matches, as East Zone lost all four matches and finished last in the tournament.

Dhoni made his Ranji Trophy debut for Bihar in the 1999–2000 season, as an eighteen-year-old. He made a half century in his debut match scoring 68* in the second innings against Assam cricket team. Dhoni finished the season with 283 runs in 5 matches. Dhoni scored his maiden first-class century while playing for Bihar against Bengal in the 2000/01 season, in a losing cause. Apart from this century, his performance in the 2000/01 season did not include another score over fifty and in the 2001/02 season, he scored just five fifties in four Ranji matches.

The Indian ODI team in the early 2000s saw Rahul Dravid as the wicket-keeper to ensure that the wicket-keeper spot didn't lack in batting talent. The team also saw the entry of wicket-keeper/batsmen from the junior ranks, with talents like Parthiv Patel and Dinesh Karthik (both India U-19 captains) named in the Test squads. With Dhoni making a mark in the India A squad, he was picked in the ODI squad for the Bangladesh tour in 2004/05. Dhoni did not have a great start to his ODI career, getting run out for a duck on debut. In spite of an average series against Bangladesh, Dhoni was picked for the Pakistan ODI series.

Dhoni's performance in the 2002–03 season included three half-centuries in the Ranji Trophy and a couple of half-centuries in the Deodhar Trophy, as he started gaining recognition for his lower-order contribution as well as hard-hitting batting style. In the 2003/04 season, Dhoni scored a century (128*) against Assam in the first match of the Ranji ODI tournament. Dhoni was part of the East Zone squad that won the Deodhar Trophy 2003–2004 season and contributed with 244 runs in 4 matches, including a century (114) against Central zone.

He was recognised for his efforts in the 2003/04 season, especially in the One Day format and was picked for the India A squad for a tour of Zimbabwe and Kenya. Against the Zimbabwe XI in Harare Sports Club, Dhoni had his best wicket-keeping effort with 7 catches and 4 stumpings in the match. In the tri-nation tournament involving Kenya, India A and Pakistan A, Dhoni helped India A chase down their target of 223 against Pakistan A with a half-century. Continuing his good performance, he scored back to back centuries – 120 and 119* – against the same team. Dhoni scored 362 runs in 6 innings at an average of 72.40 and his performance in the series received attention from the then Indian captain – Sourav Ganguly and Ravi Shastri, amongst others. However, the India A team coach Sandeep Patil recommended Dinesh Karthik for a place in the Indian squad as wicket-keeper/batsman.

Dhoni signed with Kolkata-based Celebrity management company Gameplan Sports in April 2005. Currently Dhoni has 20 endorsements, only Shahrukh Khan has more (21). In 2007 Dhoni had 17 endorsements. In July 2010, he tied up with Rhiti Sports Management and Mindscapes and was promised a minimum guarantee of Rs 210 crore over the following three years.

On the fourth day of the first Test match at Antigua Recreation Ground, St John's, Antigua during India's tour of West Indies, 2006, Dhoni's flick off Dave Mohammed to the midwicket region was caught by Daren Ganga. As the batsman started to walk back, captain Dravid declared the innings when confusion started as the umpires were not certain if the fielder stepped on the ropes and Dhoni stayed for the umpire's verdict. While the replays were inconclusive, the captain of the West Indies side, Brian Lara, wanted Dhoni to walk off based on the fielder's assertion of the catch. The impasse continued for more than 15 minutes and Lara's temper was on display with finger wagging against the umpires and snatching the ball from Umpire Asad Rauf. Ultimately, Dhoni walked off and Dravid's declaration was effected but the game was delayed, and Lara's action was criticised by the commentators and former players. Lara was summoned by the match Referee to give an explanation of his actions but he was not fined.

Dhoni is the only captain to win all ICC tournament cups- World T20 (2007), Cricket World Cup (2011) and Champions Trophy (2013).

As captain of the Indian cricket team, Dhoni has seldom been suspended due to his team's slow over rate. In December 2009, he was suspended for two ODI matches against Sri Lanka by ICC match Referee Jeff Crowe as India was three overs short of the specified rate; Virender Sehwag acted as captain for the two matches in Cuttack and Kolkata. In January 2012 Dhoni was banned for the fourth Test match against Australia in Adelaide as India was two overs short during the third Test in Perth. Sehwag captained the team in the Adelaide test and Wriddhiman Saha kept the wickets. In the CB Series in February, Dhoni again faced a one-match ban for slow-over rate against Australia.

Dhoni married Sakshi Singh Rawat, his schoolmate in DAV Jawahar Vidya Mandir, Shyamali. a native of Dehradun, Uttarakhand, on 4 July 2010. At the time of their marriage, she was studying hotel management and was working as a trainee at the Taj Bengal, Kolkata. After the retirement of Sakshi's father from his tea growing Business, their family shifted to their native place, Dehradun.

Under Dhoni's captaincy, India won the 2011 World Cup. In the final against Sri Lanka, chasing 275, Dhoni promoted himself up the batting order, coming before an in-form Yuvraj Singh. When he came to bat, India needed more than six runs per over with three top order batsmen already dismissed. He started building a good partnership with Gautam Gambhir. Due to good strokeplay and active running between wickets, they kept up with the required run rate. Dhoni was on 60 off 60 balls but later accelerated with a greater frequency of boundaries, ending with 91 not out off 79 balls. Befitting the occasion, he finished the match off in style with a huge six over long-on off Bowler Nuwan Kulasekara and won the Man of the Match award. Later in the post-match presentation, he admitted that he came up the order so as to counter the Muralitharan spin threat, as he was very familiar with Murali's bowling, who was his teammate in the Indian Premier League (IPL) franchise Chennai Super Kings. He had come after the dismissal of Virat Kohli, also a right-handed batsman. By partnering the left-handed Gambhir, he ensured a right-left combination at the crease that makes it difficult for bowlers to settle into a rhythm.

On 12 February 2012, Dhoni made an unbeaten 44 to guide India to their first win over Australia at Adelaide. In the final over, he hit a monstrous six which traveled 112 metres off the bowling of Clint McKay. During the post-match presentation, he described this six as more important than the one he hit during the ICC World Cup final in 2011.

Note – In the 2010 ICC World Twenty20, India played a Super 8 Match against West Indies. This match comes under the List of Matches played in Away Venues as the 2010 ICC World Twenty20 was being hosted in the West Indies.

He played his last series in the 2014–15 season in India's tour of Australia captaining India in the second and third tests; losing the second and drawing the third, trailing the series 2–0 before the Sydney Test. Following the third Test in Melbourne, Dhoni announced his retirement from the format. In his last Test, he effected nine dismissals (eight catches and a stumping), and in the process, went past Kumar Sangakkara in the record for stumpings with 134 (in all three formats combined). He also set a record for effecting the most dismissals in a match by an Indian wicketkeeper until it was broken by Wriddhiman Saha in 2018. He finished his last innings unbeaten making 24 runs.

The wedding took place one day after the couple got engaged. According to Bollywood Actress Bipasha Basu, a close friend of Dhoni, the wedding was planned for months and was not a spur of the moment decision. Dhoni became a father on 6 February 2015 to a baby girl named Ziva.

A biographical film based on the life of Dhoni, titled M.S. Dhoni: The Untold Story, was released on 30 September 2016.

Dhoni's final game as the Indian limited-overs captain was on 10 January 2017, in a warm-up game between England and India during the limited-overs leg of England's tour of India. Dhoni stated he will still fulfil his duties as the captain in various domestic teams.

On 18 February 2018, Dhoni created a new wicketkeeping record of having taken 134 catches in 275 T20Is against South Africa in the first T20I following the catch of Reeza Hendricks, this record was previously held by Kumar Sangakkara.

Dhoni was a part of India’s first ever Twenty20 international match. He made debut against South Africa in December 2006. He was out for a duck but India won the match. He kept the wickets and effected one catch and a run out.