Selected by the Calgary Flames with their second-round pick (57th overall) during the 2011 National Hockey League (NHL) entry draft,[8] Flames Special Assistant to General Manager Craig Conroy described Wotherspoon as a player whose qualities often go unnoticed: "If you're a stay-at-home defenceman that can join the rush, make the good first pass, doesn't get beat one-on-one, very sound, it doesn’t stand out."[1] Upon turning professional, Wotherspoon was assigned to Calgary's American Hockey League (AHL) affiliate, the Abbotsford Heat, for the 2013–14 season.[1] He had nine points in his first 48 games and a plus-minus of +13 when an injury to defenceman Dennis Wideman late in the season caused the Flames to recall Wotherspoon on an emergency basis. He made his NHL debut on March 7, 2014, a 4–3 victory over the New York Islanders.[9] He recorded his first point the following night with an assist on a Brian McGrattan goal in a contest against the Vancouver Canucks.[10] Wotherspoon appeared in 14 games with the Flames, recording four assists, before suffering a shoulder injury that required surgery and ended his season.[11] In the 2014–15 season, Wotherspoon was assigned to the Flames new AHL affiliate, the Adirondack Flames.[12] Having played 61 games with Adirondack, scoring 2 goals and 24 points, he was recalled by Calgary on April 3, 2015.[13] He made his NHL season debut in the season finale, a 5–1 loss to the Winnipeg Jets.[14] He made his playoff debut in the 2015 Stanley Cup playoffs, making four appearances in the first round win over the Vancouver Canucks, paired with David Schlemko.[15] He made two more appearances in the second round where the Flames were defeated by the Anaheim Ducks.[16][17]
Wotherspoon was assigned to the Flames' new AHL affiliate, the Stockton Heat, to start the 2015–16 season. He was recalled by Calgary in February 2016 and made his NHL season debut against the Vancouver Canucks.[18] He appeared in 53 games with Stockton, scoring 2 goals and 10 points. In 11 games with Calgary, he registered just one assist.[16] In the 2016–17 season, Wotherspoon spent the majority of the season with Stockton, playing in 56 games, netting six goals and 18 points.[19] In the 2017 Calder Cup playoffs, Wotherspoon appeared in five games for Stockon, going scoreless.[16] He also played in four games with Calgary going scoreless. On September 5, 2017, the Flames re-signed Wotherspoon to a one-year, two-way contract worth $650,000.[19] He was assigned to Stockton for the 2017–18 season after going unclaimed on waivers[20] where he put up career highs in goals (7), assists (30) and points (37) in 67 games.[16] He was named one of Stockton's associate captains for the season.[21]
After five seasons within the Flames organization, Wotherspoon left as a free agent to sign a one-year, two-way contract with the St. Louis Blues on July 1, 2018.[22] He was assigned to the Blues' AHL affiliate, the San Antonio Rampage, for the 2018–19 season.[23] He played in 70 games with San Antonio, scoring 4 goals and 22 points.[16]
On July 1, 2019, Wotherspoon signed a two-year, two-way contract with the Philadelphia Flyers.[24] He was assigned to the Flyers' AHL affiliate, the Lehigh Valley Phantoms, after going unclaimed on waivers to start the 2019–20 season.[25] He played in 54 games, scoring 4 goals and 22 points before the AHL suspended play on March 12, 2020 due to the COVID-19 pandemic.[16][26] He spent the pandemic-shortened 2020–21 season with Lehigh Valley, playing in 24 games and registering six points, all assists.[27]
On September 14, 2021, Wotherspoon signed a professional tryout contract (PTO) with the New Jersey Devils.[28] After participating in training camp and preseason, he was released from the PTO contract and signed a one-year deal with the Devils' AHL affiliate, the Utica Comets, on October 13, 2021.[27] Following a successful season with the Comets in which he scored three goals and 21 points in 53 games, Wotherspoon was signed to a two-year, two-way contract by the Devils to continue within their organization on July 13, 2022.[29] He would be assigned to Utica for the 2022–23 season and was named one of team's alternate captains.[30] Wotherspoon was again assigned to Utica for the 2023–24 season, recording four goals and 18 assists in 65 games.[31]