The following season began with Stone ranked in the top 50 on several major scouting lists for the upcoming 2010 NHL entry draft.

Suffering a concussion and thumb injury during the season, he was limited to 28 points (11 goals and 17 assists) over 39 games, hindering his final draft ranking among scouts.

Although the Wheat Kings were eliminated in the WHL Conference Finals, they advanced to the 2010 Memorial Cup by way of having been chosen as the host team at the beginning of the year.

[3] The Wheat Kings beat the Hitmen in dramatic fashion to advance to the Memorial Cup Final, which they lost to the Windsor Spitfires; Stone had no points in five tournament games.

Returning to the Senators' training camp for the second year, he was signed to a three-year, entry-level contract before being sent back to the Wheat Kings for the 2011–12 season.

[2] In December 2011, Stone was chosen as one of 16 nominees for the 54th annual H. L. (Krug) Crawford Memorial Award for sporting excellence in southwestern Manitoba.

Stone split the 2013–14 season between Ottawa and their American Hockey League (AHL) affiliate, the Binghamton Senators, recording 4 goals and 8 points in 19 NHL games.

Stone made the Senators' opening night line-up for the 2014–15 season and subsequently enjoyed success on the all-rookie "Kid Line" alongside Mike Hoffman and Curtis Lazar.

[12] As the season progressed, Stone became one of Ottawa's top-six forwards, scoring 16 goals and 43 points in his first 62 games and receiving mention as a Calder Memorial Trophy candidate as the NHL's top rookie.

On April 23, 2015, Stone was nominated for the Calder Memorial Trophy, though he ultimately finished second in voting to Florida Panthers' defenceman Aaron Ekblad.

However, unable to come to terms with the Senators on a new contract, Stone filed for arbitration and was ultimately awarded a one-year extension that would make him an unrestricted free agent the following offseason.

For his excellent two-way play during the regular season, Stone was a finalist for the Frank J. Selke Trophy as the league's best defensive forward on April 17, along with Patrice Bergeron of the Boston Bruins and the St. Louis Blues' Ryan O'Reilly.

[24] On April 14, 2019, Stone recorded his first career hat-trick to power the Golden Knights to a 6–3 victory against the San Jose Sharks in game three of the 2019 Stanley Cup playoffs.

[25] The Golden Knights were eliminated by the Sharks in seven games in the first round, with Stone recording twelve total points from six goals and six assists.

[26] The following 2019–20 season ended prematurely as a result of the onset of the COVID-19 pandemic, but the NHL subsequently arranged to hold the 2021 Stanley Cup playoffs in a bubble in Edmonton and Toronto.

[30] The postseason ended in disappointment, with the Knights reaching the semi-finals only to be defeated by the Montreal Canadiens in a series in which Vegas had been considered heavy favourites at the outset.

He returned in the closing stretch as the team attempted to salvage a playoff berth, but this came to naught and the Golden Knights missed the postseason for the first time in franchise history.

[34] He missed the remainder of the regular season, with the Golden Knights placing him on the long-term injured reserve (LTIR) list at the end of February.

[36] Stone proved a key part of the Golden Knights' deep run to the 2023 Stanley Cup Finals, where they defeated the Panthers in five games.