In sweetpotato (Ipomoea batatas), the successful emergence and development of lateral roots (LRs), the main determinant of root system architecture (RSA), determines the competency of adventitious roots (ARs) to undergo storage root formation. The present study investigated the effect of three levels of root-knot nematode (RKN) inoculum of race 3 of Meloidogyne incognita on LR length, number, area, and volume in ‘Beauregard’, ‘Evangeline’, and ‘Bayou Belle’, sweetpotato cultivars which are highly susceptible, moderately resistant, and highly resistant, respectively, to M. incognita. The three RKN levels were control (untreated), medium (500 eggs/pot), and high (5000 eggs/pot). In general, the number of galls after 20 days for each cultivar was consistent across RKN levels and two planting dates (PDs). ‘Beauregard’ inoculated with medium and high RKN levels showed 2.9 and 18.9 galls on each AR, respectively. ‘Evangeline’ had 0.5 and 3.4 galls at medium and high RKN levels, respectively. By contrast, ‘Bayou Belle’ showed only 0.9 galls at the high inoculum level. There was a significant PD × cultivar effect and cultivar × RKN level effect for all root attributes. LR attributes varied within and among resistant and susceptible cultivars with a general trend for increase in all root growth attributes in response to RKN infection in the first (PD1) and second PD (PD2). ‘Evangeline’ showed relatively consistent within-cultivar increase across PD1 (medium and high RKN levels) and PD2 (medium RKN level only). LR length, number, area, and volume within ‘Evangeline’ plants subjected to high RKN increased 122%, 126%, 154%, and 136%, respectively, relative to the untreated control plants in PD1. ‘Evangeline’ (PD1 and PD2) and ‘Bayou Belle’ (PD1 only) showed significant increase in all root attributes relative to the susceptible ‘Beauregard’ at medium or high RKN levels. In PD1, LR length, number, area, and volume in ‘Evangeline’ plants subjected to high RKN increased 165%, 167%, 176%, and 190%, respectively, relative to ‘Beauregard’ plants at the same RKN level. These findings are consistent with some data in other systems wherein nematode infection is associated with cultivar-specific root compensatory growth and demonstrate how genotype and environment interact to modify root development responses. These data can be used to further understand the role of cultivar-specific responses to nematode infection and can lead to the consideration of root traits in selection strategies.