He plays for Tamil Nadu and South Zone in domestic cricket and for Chennai Super Kings in the Indian Premier League (IPL).

Ashwin started as an opening batsman but dropped down the order due to limited success and turned into an off-break bowler.

He played for the Chennai Super Kings (CSK) in the 2010 Indian Premier League, where his economical bowling led to his maiden international call-up in the limited-overs formats in June 2010.

[9] Ashwin started playing cricket at the age of nine for YMCA and was coached by Chandrasekar Rao during the early part of his career.

[17] He was also part of the tri-series against New Zealand and Sri Lanka, but did not get a game, with Pragyan Ojha and Ravindra Jadeja being preferred.

[21] Despite being in the squad, Ashwin did not make it to the playing eleven in any of the five ODIs on the South African tour in 2010, with Harbhajan Singh preferred.

[26] Ashwin was retained in the limited-overs squad for the England tour and emerged as India's best bowler of the series, taking six wickets at an average of 25.16.

[28][29] In November 2011, West Indies toured India for three Tests and five ODIs, with Ashwin and Ojha being the only two specialist spinners in the squad.

[61][62] With nine wickets in six matches, Ashwin finished as the leading wicket-taker of the home ODI series against Australia in October–November 2013, which India won 3–2.

[65] In early 2014, Ashwin's overseas struggles continued during the New Zealand tour, where he managed to bag a solitary wicket in the five-match ODI series, which India lost 4–0.

[68] In the two-match Test series that followed, Jadeja was preferred over Ashwin as the lone spinner in the playing eleven.

[91] Ashwin followed it up with an all round performance, taking 28 wickets and scoring 306 runs in the five match test series against England, which India won 4–0.

[99] Ashwin was part of the limited overs squad that toured West Indies in June 2017 after which he became a player who played exclusively in tests.

[26][110] In the following series in the Indian tour of Australia, India won a historic 2–1 victory, with Ashwin taking 12 wickets across three matches.

[113] Ashwin was the lead wicket-taker with four wickets in the 2021 ICC World Test Championship final loss to New Zealand in June 2021.

[114] In September 2021, Ashwin earned a surprise recall to the Indian squad for the 2021 ICC Men's T20 World Cup, more than four years since he played a T20 international.

[115] He made the comeback in white-ball cricket in India's third match of the tournament against Afghanistan and bowled a good spell taking two wickets for 14 runs in four overs.

[43] He was also named in the Indian squad, which reached the semi-finals of the 2022 ICC Men's T20 World Cup, playing all six matches and taking six wickets.

[124] Ashwin earned a surprise recall to the ODI side for the series against Australia prior to the 2023 Cricket World Cup, in which he took four wickets from two matches.

This was the fourth time he did a double of scoring a century and taking more than five wickets in a test match, and became the first cricketer to achieve the feat twice at the same venue.

[31] Ashwin made his first class debut for Tamil Nadu in the Ranji trophy match against Haryana in 2006 at the age of 20, taking six wickets.

[140] Ashwin captained the Tamil Nadu team that won the Vijay Hazare Trophy in 2008-09 and reached the semi-finals in 2015.

[146] Ashwin was drafted in as the captain of the Dindigul Dragons franchise for the inaugural season of the Tamil Nadu Premier League (TNPL) T20 tournament.

[154] Ashwin was signed as a domestic player by Chennai Super Kings (CSK) for the inaugural season of the Indian Premier League (IPL) in 2008.

[157] His break through season came in 2010 when he took 13 wickets to help Chennai win their first IPL title and qualify for Champions League Twenty20.

[157] Following the two-year suspension of Chennai Super Kings and Rajasthan Royals, two new franchises Rising Pune Supergiants and Gujarat Lions were established for the 2016 Indian Premier League season.

[165] In March 2019, in a match against Rajasthan Royals, Ashwin ran out a batter "backing up" (Jos Buttler), reigniting a debate around the mode of dismissal.

[171] During the group stage match against Lucknow Super Giants in the 2022 season, he tactically retired out in the 19th over, becoming the first cricketer in IPL to do so.

[31] However, he has stated in an interview that he refrains from bowling the doosra as it requires him to bend and straighten his arm which he finds difficult to do.

[247] In June 2024, Ashwin released his memoir titled I have the streets: A kutti cricket story, which he had co-authored with sports writer Sidharth Monga.