He won back-to-back Stanley Cup championships with the Penguins in 2016 and 2017 and is the fourth longest tenured member of the organization aside from Sidney Crosby, Evgeni Malkin, and Kris Letang.

Rust won a gold medal at the 2010 IIHF World U18 Championships for Team USA and the 2013 CCHA Tournament for Notre Dame.

[2] Rust officially concluded his collegiate career on April 1, 2014, after signing a two-year entry-level contract with the Pittsburgh Penguins.

[6] This continued into the regular season and Rust quickly found himself on the Penguins top line with Tom Kostopoulos and Nick Drazenovic.

[7] Rust remained in the AHL for the first half of the season before earning his first NHL recall on December 4 to replace an injured Scott Wilson.

He was returned to the WBS Penguins without making his NHL debut on December 6 and immediately tallied three points in his first game back.

[4] Rust remained sidelined until May 9 when he returned to the WBS Penguins for Game 3 of the Calder Cup playoffs against the Manchester Monarchs.

[22] While he was returned by the end of the month, Rust was recalled to the NHL level again on January 7 after adding one goal and two assists to his points total.

[23] Rust remained at the NHL level until the team acquired forward Mark Arcobello off waivers from the Predators on January 14.

[30] Rust returned to the Penguins lineup for their First Round series against the New York Rangers in the 2016 Stanley Cup playoffs and joined Malkin and Sheary on the third line.

[31] In Game Five, Rust scored two goals and added an assist to help the Penguins record a four-goal second period.

His first two goals of the postseason helped the Penguins eliminate the Rangers in five games and advance to the Eastern Conference Second Round.

[29] Following the Stanley Cup win, it was revealed that Rust had played through a broken finger in Game 6,[38] but a more complicated injury delayed his return for the 2016–17 season.

[40] While he was originally expected to play on the right wing of Malkin, he ended up spending most of the season on Nick Bonino's line or with Sidney Crosby and Conor Sheary.

[41] During the Penguins first round series against the Columbus Blue Jackets, Rust joined Malkin and Phil Kessel as linemates on their second line.

[45] On April 20, Rust scored two pivotal goals, including the game-winner, in Game 5 to lift the Penguins to a series win.

[47] His momentum would stall during the Penguins Eastern Conference Final series against the Ottawa Senators after he was injured by defenceman Dion Phaneuf in Game 2.

As teammates Conor Sheary and Patric Hörnqvist were out due to an injury, Rust joined Nick Bonino and Carter Rowney on the third line.

[55] After missing nearly a month to recover, Rust made an immediate impact on the lineup by tallying four goals and seven points through his first seven games back.

[56] He earned praise from head coach Mike Sullivan who called him a swiss army knife and a versatile player who could play "up and down the lineup.”[57] Although Rust experienced a dip in scoring, he set new career-highs in assists with 25 and points with 38.

[59] After the Penguins fell in the second round to the Washington Capitals, Rust signed a four-year $3.5 million contract extension to remain with the team.

[66] Despite his slow start, Rust accumulated a career-high 17 goals before suffering a lower-body injury during a game against the Columbus Blue Jackets on February 26.

[78] On March 3, Rust recorded his third career NHL hat-trick to help the Penguins end a six-game losing streak with a 7–3 win against the Ottawa Senators.

[81] They rejoined the Penguins when the NHL started its return-to-play initiative for the 2020 Stanley Cup playoffs and played against the Montreal Canadiens in the Eastern Conference Qualifying Round.

[89] On March 27, Rust recorded his fourth career NHL hat-trick to lift the Penguins 6–3 over the New York Islanders and extend his point streak to six games.

[94] Due to their first place finish, the Penguins met with the New York Islanders in the 2021 Stanley Cup playoffs East Division First Round.

During a game against the San Jose Sharks, Rust and Evan Rodrigues each recorded a hat-trick in the third period to lift the Penguins to an 8–5 win.

[101] In spite of this gap, Rust was named the NHL's Third Star of January after he finished the month with 10 goals and 11 assists through 11 games.

On December 6, Rust suffered an upper-body injury during a loss to the Tampa Bay Lightning and was expected to miss at least a week to recover.