Ray spent the majority of his professional career with the Edmonton Eskimos and Toronto Argonauts of the Canadian Football League (CFL).

He also set several school records during his time at Shasta, most notably throwing 199 consecutive pass attempts without allowing an interception.

He earned the nickname "Frito Ray" by teammates, as he was working as a delivery driver for Frito-Lay chips when he was called up for training camp.

The failure forced the Eskimos into an onside kick attempt, which failed as Montréal returned it for a touchdown and took a lead that they would not lose.

Despite splitting time early in the year, Ray ended with a 67.6 completion percentage, 4,640 yards, 35 touchdowns and 13 interceptions and was a candidate for the Most Outstanding Player award.

The Eskimos rebounded from their slow start and made the playoffs, defeating the Saskatchewan Roughriders in the Western final as Ray threw for 356 yards.

Ray played exceptionally against Alouettes coach Don Matthews's renowned blitzing defense, completing 22 of 32 passes for 301 yards and two touchdowns.

But the lure of the league he had dreamed of in his youth proved too strong to keep Ray in Canada, and he signed with the New York Jets.

When starter Chad Pennington went down briefly with a rotator cuff injury, backup Quincy Carter came in and played well, relegating Ray to the bench.

However, towards the end of the year, Ray's play faltered, concluding in him not throwing a touchdown in the season's last four games.

Head coach Danny Maciocia, however, promised Ray the start in the 93rd Grey Cup, perhaps because of rumours that a trade of Maas to the Hamilton Tiger-Cats had already been arranged.

The Eskimos defeated the Montreal Alouettes 38–35 in overtime, and Ray was named most valuable player of the Grey Cup.

In 2006, Ray started for the Eskimos for every single game of the season, led the league in passing with exactly 5,000 yards, and was near the top in completion percentage at 65.7%, 21 touchdowns, and a passer rating of 89.8.

On September 14, 2007, in a win against the Montreal Alouettes, Ray surpassed CFL and NFL hall-of-famer Warren Moon to capture the Eskimos' all-time record for career passing yards.

[7] On September 28, 2007, he suffered a separated shoulder at the hands of Toronto Argonauts safety Willie Pile, ending his season.

He led the Esks to a win in the crossover playoff game in Winnipeg, but the team lost in the East finals to Montreal.

Ray was traded to the Toronto Argonauts on December 12, 2011, for quarterback Steven Jyles, placekicker Grant Shaw, and a 2012 first round draft pick.

[13] Ray would return for the final two games of the season completing 20 of 33 passes for 383 yards, 4 touchdowns and no interceptions vs Winnipeg and 24 of 30 passes for 305 yards, 4 touchdowns and 1 interceptions against Saskatchewan, earning offensive player of the week honors[14] for the latter performance and helping the Argos clinch a playoff spot.

In the first game of the season against Hamilton, Ray complete 24 of 34 passes for 368 yards, 4 touchdowns and no interceptions, earning him offensive player of the week honors.

[31] Ray would earn his second offensive player of the week honors after completed 30 of 35 passes for 413 yards with 3 touchdowns and no interceptions against Edmonton in game 6.

[33] In spite of the personal spectacular regular season, Ricky Ray leading the Argonauts to a first-place finish in the East would be ruined by Henry Burris and the Hamilton Tiger-Cats defeating Ray and the Argonauts 36–24 in the 2013 East Division final held at the Rogers Centre, Toronto.

In November 2014, following the conclusion of the Argos season, Ray had surgery to repair a torn labrum in his right (throwing) shoulder and a small tear in his right rotator cuff.

In the playoff game Ray completed 22 of 34 pass attempts for 220 yards with 1 touchdown and 1 interception; however Justin Medlock kicked a 47-yard field goal with no time on the clock to eliminate the Argos, thus ending their season.

Ray started the first five games of the season before sustaining a knee injury as defensive lineman Vaughn Martin rolled up into him in the third quarter.

Following their Labour Day game against the Tiger-Cats, reports surfaced suggesting Ray would miss the remainder of the 2016 CFL season with a punctured lung.

However, he was unable to best the league-leading Stampeders and as a result the Argos were eliminated from playoff contention, falling to a record of 5–12.

On October 21, 2017, Ray reached the 60,000 career passing-yard mark, becoming just the fourth player in CFL history to accomplish the milestone.

For his performance, Ray finished as runner-up to Edmonton quarterback Mike Reilly for the CFL's Most Outstanding Player Award.

[56] By early March Ray had not informed the Argos of his intentions for the 2019 season, and still needed to be cleared by doctors before returning to the field.

General manager Jim Popp hinted that if Ray were to return to the Argos it would be as a backup quarterback, possibly transitioning to a coaching role in the future.