College and amateur Johnson grew up in
Lilburn, Georgia, where he attended
Brookwood High School. For a brief period he attended school in California where he played for his high school in Los Angeles County. He would graduate from there in 2005. Johnson moved to
Florida to play
college soccer at the
University of Central Florida, where he earned Member of the C-USA Commissioner's Honor Roll and was named Team MVP in 2008. He left college early to enter the
2010 MLS SuperDraft as a
Generation Adidas player. During his college years Johnson also played one season with
Atlanta Blackhawks in the
USL Premier Development League.
Professional Sean Johnson was drafted in the fourth round (51st overall) of the
2010 MLS SuperDraft by
Chicago Fire. He was the last Generation Adidas player selected in that draft. He made his MLS debut on August 1, 2010, during a 3–2 victory over
Los Angeles Galaxy after earning the starting spot over
Andrew Dykstra. In his rookie season, he earned back to back "Save of the Week" honors. In 2013, he was named the Chicago Fire's Defender of the Year. He had an 11–9–7 record with the Fire, including with 6 clean sheets. On December 11, 2016,
Atlanta United acquired Johnson from the
Chicago Fire for general allocation money. Later that day
New York City FC acquired Johnson from Atlanta United in exchange for general allocation money and target allocation money. He made 206 total appearances for NYCFC and won the
2021 MLS Cup with the club as their starting goalkeeper. On January 27, 2023, Johnson signed a two-year contract with
Toronto FC. Following the 2025 season, Johnson became a free agent. On December 23, 2025, Johnson signed a contract with
D.C. United through June 2027. ==International career==