Richmond (9-3) which has won seven consecutive games since a 2-3 start, advances to play Saturday at fifth-seeded Albany (9-3), which shared the Coastal Athletic Association with the Spiders and automatic qualifier Villanova (9-2), the eighth seed. Only the top eight teams in the 24-team FCS playoffs are seeded.
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The Spiders' 49 points were the most in postseason play for the program since the 1968 Tangerine Bowl.
The loss spoiled the Eagles' playoff debut.
Smith's 14-yard scoring run with 10:07 left in the third quarter put Richmond up 21-20, and with the game in the balance, his 65-yard punt return for a touchdown to close out the quarter served as the catalyst to send Richmond to what became a comfortable win.
Wickersham threw a 71-yard score to Jerry Garcia Jr. to make it 35-20, but NCCU quarterback Davius Richard helped engineer a six-play, 75-yard drive and the Eagles reduced the deficit to 35-27 when he ran it from the 2 with 9:54 remaining. Richmond responded when Garcia ran it in from 7 yards out at the end of a seven-play, 60-yard drive.
Richmond got on the board first when Wickersham threw a 35-yard score to Nick DeGennaro three plays in.
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The Eagles rallied when Richard sandwiched scoring runs of 1 and 18 yards around a 91-yard scoring throw to Devin Smith to close the first quarter with a 20-7 lead. Richard threw for 262 yards, a touchdown and an interception. He ran for 79 yards on 18 carries and scored three touchdowns.
The 91-yard strike ranks as the fourth-longest passing TD in NCCU program history, and was the longest of Richard's career, besting his 86-yard mark that he set on a completion to Quentin McCall against Winston-Salem State earlier this year.
Richmond's Smith got his third touchdown, ending the scoring with his 24-yard run with 3:33 left.
North Carolina Central, which moved from Division II to Division I in 2011, made its first appearance in the FCS playoffs after finishing second in the Mid-Eastern Athletic Conference.
Richard finished his career with 11,017 total yards. Defensively, Jayden Flaker notched a game-high 11 tackles to lead the Eagles, and Quantez Mansfield had 1.5 tackles for loss with 0.5 sacks and a blocked field goal in the first half.