Dhoni achieved the milestone during the third and final Twenty20 International against Zimbabwe at the Harare Sports Club.
India won the series 2-1, days after 3-0 whitewash of the hosts in ODIs.
Dhoni, who was appointed captain in 2007, has led India in 60 Tests, 194 ODIs and 70 T20 Internationals.
The 34-year-old is also India’s most successful captain ever, having overseen 27 Test match victories, 107 ODI wins and 40 T20 successes.
During his nine-year tenure, Dhoni has guided India to title triumphs in the World T20 (2007), the World Cup (2011) and the Champions Trophy (2013) besides leading the side to the top of the ICC Test rankings.
Now leading India in ODIs and T20s, the veteran wicketkeeper-batsman had retired from Test cricket in 2014 in the middle of a high-profile series in Australia.