He had his first, limited playing time in 1998 in relief of Jeff Garcia and Dave Dickenson, while dressing for all of the Stampeders' games. In 1999 he received more playing time as Dickenson's backup. He replaced Dickenson in the third week game against the Edmonton Eskimos, leading the Stampeders to a come-from-behind victory. He started the following two games against the Montreal Alouettes and BC Lions, leading the Stampeders to another victory in the former. He was injured in the third quarter of the latter, and spent the rest of the season on the injured reserve with a torn anterior cruciate ligament.
He moved on to the Saskatchewan Roughriders for his first opportunity to be a full-time starting quarterback. He started the first 16 games of the Roughriders season, throwing for 4,647 yards and 30 touchdowns.
The Green Bay Packers took interest in him after the CFL season ended, and signed him to a contract. Burris began playing in the NFL in 2001, when he spent several weeks as the Packers' third-string quarterback, before he was released and spending the rest of the season on their practice squad.
He was signed by the Chicago Bears in the off-season. In six games for the Bears he completed 18 of 51 passes for 207 yards, with three touchdowns and five interceptions. He received significant playing time only in the last two games of the regular season. He was 8 of 22 for 50 yards and a touchdown against Carolina, fumbling twice, and 7 of 19 for 78 yards and four interceptions against Tampa Bay, for a 10.3 QB rating. While his passing was quite poor he showed better than average running ability for a quarterback, finishing the 2002 season with 15 rushes for 104 yards.
The Bears assigned him to NFL Europe's Berlin Thunder in 2003 where he performed respectably. Unhappy with being relegated to Berlin by the Bears, he returned to the CFL and the Roughriders, his former club. He immediately became Nealon Greene's back-up. A knee injury forced him to miss the better part of the season.
In the off-season Burris rejected the Roughriders' contract offer in order to re-join the Calgary Stampeders. In 2005 he took the Stampeders to the Western Semifinal, where they lost at McMahon Stadium to Ricky Ray and Jason Maas of the Edmonton Eskimos. In 2006 he once again helped the Stampeders advance to the CFL playoffs, hosting their second home playoff game in as many years, but lost in the West Semifinal to his former team, the Roughriders.
In the 2007 playoffs the Stampeders once again faced off against the Roughriders in the Western Semifinal (this time played at Mosaic Stadium in Regina, where the Roughriders were hosting their first home playoff game since 1988). Burris once again lost to his former team in a close 26–24 affair.
In 2009, Burris led the Calgary Stampeders to a second-place finish in the Western Conference. Trying to atone for a year in which he could not beat the first place Saskatchewan Roughriders (0–3–1), the Burris led Stampeders could not defeat the Roughriders in the Western Division Final, falling 27–17. This was Burris' third straight play-off loss to the Roughriders.
Burris quarterbacked the Stampeders to a CFL best record of 13–5 in 2010, finishing first in the Western Conference. Looking for revenge against his play-off nemesis, Burris lost to the Roughriders for the fourth time in the post season, 20–16. He won the CFL's Most Outstanding Player award for that season.
Burris' string of professional starts ended at the end of the 2011 season, when Drew Tate replaced him as the starting quarterback for the last three scheduled regular season games. Burris performed short-yardage duties for the team as the back-up quarterback. Burris returned to quarterbacking the Calgary Stampeders in the second half of the Western Conference Semi Finals against the Edmonton Eskimos. Burris was unable to lead a second half comeback throwing only 7 completions in 15 attempts with 0 touchdowns, having to settle for multiple field goals.
Entering the off-season there had been much speculation regarding the future of Burris with the Calgary Stampeders. The Stampeders seemed ready to move on and hand the starting job to Drew Tate while Burris had stated that he did want to be a backup quarterback. The Calgary Stampeders confirmed on January 3, 2012 that they had traded Burris to the Hamilton Tiger-Cats for QB Kevin Glenn and OL Mark Dewit.
Henry Burris, photographed at Investors Group Field in Winnipeg, Manitoba on November 2, 2013 playing in the last regular season game of the Hamilton Tiger-Cats for the 2013 CFL season.
In his first season with the Tiger-Cats, Burris had a career year. He threw for 5,367 yards and 43 touchdowns, with a passer rating of 104.4, all career highs. Unfortunately, the Tiger-Cats defense struggled, giving up an average of 32 points per game, which resulted in the team falling to 6–12 and missing the playoffs.
On September 13, 2013, midway through the 2013 CFL season, Burris became the 5th CFL quarterback to throw for 50,000 career passing yards. Burris' 4,925 passing yards was enough to lead the league in passing for the second consecutive year. Burris led the Tiger-Cats into the post-season with a record of 10–8, they defeated the Montreal Alouettes and then the Toronto Argonauts, but ultimately lost to the Saskatchewan Roughriders in the 101st Grey Cup game. Entering the off-season, Burris was set to become a free-agent in February 2014 unless he re-signed with the Tiger-Cats. He expressed his desire to stay with the Ti-Cats, saying, "I want to be back here, we've had a great run. I still feel like I can get it done." However, Burris was released by Hamilton on January 30, 2014, following the signing of Zach Collaros.
On February 4, 2014, Burris signed a three-year contract with the Ottawa Redblacks. The 2014 CFL season was Burris' worst season statistically since his 2003 year with the Roughriders. Burris led the inaugural season of the RedBlacks to a 2–16 record. His completion percentage was his lowest since 2009, and only managed to score 11 touchdowns in 18 games, while throwing 14 interceptions. On October 1, 2015, Burris set an new CFL record for completions in a game connecting on 45 passes for a career high 504 passing yards. On November 7, 2015, Burris became the CFL's record holder for most completions in a season with 481 completions. Additionally, Burris finished the 2015 season as the league leader in passing yards and completion percentage. He led the RedBlacks to a record of 12–6, earning a first round bye in the process. In the Eastern Final Burris lead the Redblacks over his old team the Tiger-Cats, personally advancing to the Grey Cup for the second time in three seasons. Prior to the Grey Cup game Henry Burris was named the CFL's Most Outstanding Player for 2015.