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Okello was named to the Canadian U-23 provisional roster for the 2020 CONCACAF Men's Olympic Qualifying Championship on February 26, 2020.

Okello made his senior debut on January 7, 2020 against Barbados as a substitute in a 4–1 victory.

Okello was promoted to the Toronto FC first team on 22 January 2019. He made his first-team debut for Toronto on August 14 against the Ottawa Fury in the second leg of their 2019 Canadian Championship semi-final series.

Okello was named to the Canadian senior team's provisional 40-man roster for the 2019 CONCACAF Gold Cup He was named to the final squad on May 30.

Following the conclusion of USL season Okello was invited to train with VfL Wolfsburg. On 10 January 2018, he played a full 90 minutes for their U19 side in a 2–1 victory over Hallescher FC where he scored the equalising goal in the 88th minute On 13 January 2018, he played in the 4–1 win over BFC Dynamo at the Porschestadion and Thomas Reis described his performance as enthusiastic and satisfying. He was recalled by his club to take part in first team pre season with 2017 MLS champions Toronto FC in Los Angeles starting on 22 January 2018.

He made his first team debut on 31 January 2018 in a pre season friendly against Tijuana coming on in the 61st minute to replace Michael Bradley in central midfield as the team was winning 3–2. The game finished in a 3–2 victory for Toronto. On 2 February 2018, he started against Los Angeles FC in their first ever pre season game at Drake Stadium (UCLA) which finished 2–2. On 6 February 2018, he travelled with the first team to Mexico for the second leg of their 2018 pre season with games scheduled against Liga MX clubs Pachuca, América and Cruz Azul.

On 6 April 2018, it was reported that VfL Wolfsburg had made three separate transfer bids to sign the player which would see his club receive a six figure transfer fee in addition to appearance fees and sell on percentage fee. Toronto FC confirmed that an offer was received yet did not clarify why the bid was rejected.

On 18 April 2018, he made his first start of the 2018 USL season playing the full 90 minutes and helping his team pick up its first points of the season and clean sheet in a 0–0 draw at BMO Field. He finished the game with an 87.3% pass success rate.

On 16 September 2018, he started and played the full 90 minutes in front of 27,275 fans at Nippert Stadium against FC Cincinnati in a thrilling game that finished 4–3.

In May 2018, he was called up to the Canadian U23 side for the 2018 Toulon Tournament. On 28 May 2018, he started in the Group C game against Portugal U20 which finished 0–0. In October 2018, Okello was named to the Canadian U20 squad for the 2018 CONCACAF U-20 Championship. He scored a brace in the tournament opener against Dominica, a 4–0 victory.

Born in Toronto, Ontario, Okello was part of the Toronto FC youth system since the age of 12. On 20 August 2017, he was part of the U17 side that beat Juventus U17 to capture the inaugural International Youth Soccer Cup in dramatic fashion. He played 16 games for TFC Academy during the 2016 season and 13 games during the 2017 season, scoring once against ProStars FC. On 15 September 2017, Okello signed his first professional contract. On 6 October 2017, he made his professional debut against Bethlehem Steel FC in the USL replacing Brian James in the 71st minute.

Okello has represented Canada U17 and was part of their 2017 CONCACAF U-17 Championship campaign coached by former Werder Bremen and Tottenham Hotspur full back Paul Stalteri.

Because of his height, technical ability and range of passing Okello has been likened to Paul Pogba. The TFC Prospect report and Greg Vanney describes him as having the "ability to control the ball and play short, long and fast whilst under pressure. He is calm and little seems to faze him. When Okello roams, he is capable of covering a lot of ground — with or without the ball — quickly. His technique with both feet enables him to glide past opponents without breaking stride".

Noble Okello Ayo (born 20 July 2000) is a Canadian professional footballer who plays as a midfielder for Toronto FC in Major League Soccer.