Miller made his first-class debut in the Dolphins' final game of the 2007–08 domestic SuperSport Series, scoring a half-century in the first innings in which he batted. Miller made eight appearances in the one-day MTN Domestic Championship competition of the same season, though his final match was abandoned after just three overs. Miller scored an average of 13 runs throughout the competition, which saw the Dolphins finish in fifth place in the league. Miller played two matches in the Pro20 Series Twenty20 competition for the Dolphins, who finished as defeated finalists in the competition. In May 2018, he was named as one of the ten marquee players for the first edition of the Global T20 Canadacricket tournament. On 3 June 2018, he was selected to play for the Winnipeg Hawks in the players' draft for the inaugural edition of the tournament. In October 2018, he was named in Durban Heat's squad for the first edition of the Mzansi Super League T20 tournament. In September 2019, he was named in the squad for the Durban Heat team for the 2019 Mzansi Super League tournament.
Indian Premier League
In the 2013 IPL Auctions Kings XI Punjab bought Miller for ₨ 6 crore. He went on to play all the matches for his team that season. On 6 May 2013, Miller hit the third fastest hundred in IPL history. He scored 101 not out off 38 balls whilst chasing against Royal Challengers Bangalore at the IS Bindra Stadium, Mohali. The opposing captain Virat Kohli, who dropped a catch when Miller was on 41, said of the innings that it was one of the best innings he had ever seen in the Indian Premier League history. He was retained by Kings XI Punjab for 2014 IPL where he played all matches and help his team to reach the finals. It was announced that he will be the Captain of the Kings XI Punjab for 2016 IPL. After Kings XI Punjab lost five of their first six games, he was dropped as the captain and was replaced with Murali Vijay. During IPL 2015 season in the match between Kolkata Knight Riders and Kings XI Punjab at Eden Gardens on 9 May, a policeman was left with his left eye blind after a ball struck him after being hit for a six by David Miller. He was released by the Kings XI Punjab ahead of the 2020 IPL auction. In the 2020 IPL auction, he was bought by the Rajasthan Royals ahead of the 2020 Indian Premier League.
International career
Miller earned his national call-up in May 2010 after a series for South Africa A against Bangladesh A, where he ended as the second-highest run-scorer. Miller made his Twenty20 International debut for South Africa on 20 May 2010 against the West Indies in Antigua. Miller, called up to replace the injured Jacques Kallis, dispatched the sixth ball of his innings for six and went on to top score as South Africa won by just 1 run. Two days later Miller made his ODI debut, also against the West Indies. He put in another good performance, scoring 23 not out and helping South Africa to victory. Miller was selected to play in Zimbabwe's tour of South Africa, during which he contributed in both ODI and T20 formats towards a resounding victory by the South Africans. He was then selected for the squad to play Pakistan in the U.A.E. during October and November 2010. He played in two ODI series, against West Indies and Pakistan, before being named in South Africa preliminary 2011 World Cup squad. On 15 October 2010, Miller made his maiden ODI fifty against Zimbabwe and South Africa went on to put a massive total of 351. Miller was a part of the South African team for the tour of Sri Lanka in July 2013 where in the 3rd ODI he scored 85* off 72 balls and gave South Africa their first win of the tour. Miller also won the Man of the Match title. In the semi-finals of the 2013 ICC Champions Trophy he along with Rory Kleinveldt set the record for the highest 9th wicket partnership in ICC Champions Trophy history, with 95. Miller made his Maiden One Day International century in the 4th ODI against the West Indies on 25 January 2015. In August 2017, he was named in a World XI side to play three Twenty20 International matches against Pakistan in the 2017 Independence Cup in Lahore.
Miller was one of South Africa's top performers at the 2015 Cricket World Cup scoring 324 runs at an average of 65 and strike rate of 139 during the tournament. He scored 49 off 18 balls in the semi final, although his effort was in vain as New Zealand won the match. During that World Cup he along with JP Duminy set the record for the highest 5th wicket partnership in ODI history as well as World Cup history.
2017–18 Bangladesh series
On 15 October 2017 he played in his 100th ODI and became the third player after Rohit Sharma and Kieron Pollard to play 100 ODIs without featuring in a Test match. In the 2nd T20I of the same tour he scored his first century in a T20I and made the fastest century in a T20I. He was also the first player to score a T20I century batting at number five or lower. During this match he became fifth player from South Africa to score 1,000 runs in T20Is.
In April 2019, he was named in South Africa's squad for the 2019 Cricket World Cup. On 19 June 2019, in the match against New Zealand, Miller scored his 3,000th run in ODIs.
