The son of a former boxing champion, Newbiggin-by-the-Sea, Northumberland born centre forward Ernie Thompson began his football career with Consett in 1924 and Stakeford United in 1926. In August 1928, he had trials with Third Division North sides Ashington and Carlisle United, and Second Division Bradford Park Avenue. After declining terms with Ashington, he signed as an amateur with Third Division (North) Carlisle before turning professional three weeks later in September 1928, making his Football League debut at Wigan Borough in February 1929, scoring in a 2-2 draw. His only other appearance came a week later in a 1–0 home win over Crewe Alexandra and he spent most of the 1928-29 season in the club’s reserve team, scoring 26 goals as the team won the North Eastern League Second Division and the Cumberland Cup.
At the end of the season, Thompson joined Second Division Bristol City, but never made a first-team appearance, instead spending his single season with the club playing in the reserves in both the Western Section of the Southern League and the Western League First Division. He left before the end of the 1929-30 season in February 1930 to join Bath City, playing for them in the Southern League for just over a year before joining First Division side Blackburn Rovers in April 1931.
He scored on his Blackburn Rovers debut in a 1-6 defeat to Sheffield Wednesday in August 1931, and scored his first hat-trick for the club in a 5-1 win at Aston Villa that December. A “bustling, forceful centre-forward”, he was Blackburn’s leading scorer in four of his five full seasons at the club. In 1936, Blackburn were relegated to the Second Division, but Thompson was presented with the opportunity to return to the First Division when he signed for Manchester United for a fee of £4,500 in November 1936 after 84 goals in 179 appearances for Rovers. He scored on his debut at home to Liverpool on 21st November, but the match ended in a 5-2 defeat. He played again in the next game away to Leeds United on 28th November, but didn’t manage to score and Manchester United lost 2-1 on their way to relegation from the First Division.
He only made one more appearance for the club the following season, in a 2-1 defeat at home to Southampton on 25th September 1937, before joining Gateshead in March 1938, where he scored twice on his debut in a 4-1 win over Halifax Town. After just over a year with Gateshead, during which time he scored a total of 7 goals in 26 appearances, Thompson joined York City in the 1939 close season. He scored in his second appearance for the club, a penalty in a 2-1 defeat away to Rotherham United, but his time there was cut short by the outbreak of the Second World War, after just three appearances for The Minstermen, and he retired during the War.