He had also been a talented junior tennis player, but eventually chose to pursue cricket.

He played for Victoria at both under-17 and under-19 level, and went on to play for the Australian under-19 cricket team during the Sri Lankan under-19 team's tour of Australia in October 2009.

Having spent the 2011 season playing English club cricket for Tring Park, as well as several matches for Leicestershire in the Second XI Championship. Handscomb debuted for Victoria during the 2011–12 Australian season, playing as a top-order batsman. He scored 42 and 71 runs, respectively, in his first List A and first-class innings, both in matches against Queensland at the Gabba. Handscomb's first century in Sheffield Shield matches came against South Australia in February 2012, an innings of 113 runs at the Adelaide Oval. Towards the end of the season, he was also used as Victoria's wicket-keeper, with both Matthew Wade and Ryan Carters unavailable. Handscomb was awarded Cricket Victoria contracts for both Victoria and the Melbourne Stars for the 2012–13 season. In Victorian Premier Cricket, he plays for the St Kilda Cricket Club, and led the club's batting averages during the 2011–12 season. Handscomb also holds British citizenship, with both of his parents English immigrants to Australia.

Handscomb's break-through first class season occurred for Victoria in 2014–15, when he scored three centuries and averaged 53.91. He played county cricket for Gloucestershire during 2015, and began touring with Australia A, becoming captain of the team in early 2016.

In November 2016, immediately after his maiden first-class double century against New South Wales and amidst the backdrop of Australia's disastrous home series loss against South Africa and the retirement of chairman of selectors Rod Marsh, Handscomb was one of several players brought into Australia's Test team ahead of the dead rubber third Test against South Africa.^[12] He made his Test debut on 24 November 2016,^[13] and was presented his baggy green cap by Chris Rogers.^[14]

Batting at number five, Handscomb made an impressive start to his Test career, scoring 399 runs at an average of 99.75 across the remaining four home Tests of the summer: one against South Africa and three against Pakistan. He scored his maiden Test hundred (105) in the first Test against Pakistan at the Gabba, in a 172-run partnership with skipper Steve Smith,^[15][16] and followed it with 110 in the third Test at the Sydney Cricket Ground.Peter Handscomb became the first batsman in history to score his maiden test century in a Day Night test match. With half-centuries in the other two matches, Handscomb became the second Australian Test cricketer to score a half century in each of his first four Tests,^[17] and was not dismissed for less than fifty in any innings.

He made his One Day Internationals (ODI) debut in Perth on 19 Januar