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Antimicrobial resistance associated with the spread of plasmid-encoded extended-spectrum β-lactamase (ESBL) genes conferring resistance to third generation cephalosporins is increasing worldwide. However, data on the population of ESBL producing <i>E. coli</i> in different animal sources and their antimicrobial characteristics are limited. The purpose of this study was to investigate potential reservoirs of ESBL-encoded genes in <i>E. coli</i> isolated from swine, beef, dairy, and poultry collected from different regions of the United States using whole-genome sequencing (WGS). Three hundred isolates were typed into different phylogroups, characterized by BOX AIR-1 PCR and tested for resistance to antimicrobials. Of the 300 isolates, 59.7% were resistant to sulfisoxazole, 49.3% to tetracycline, 32.3% to cephalothin, 22.3% to ampicillin, 20% to streptomycin, 16% to ticarcillin; resistance to the remaining 12 antimicrobials was less than 10%. Phylogroups A and B1 were most prevalent with A (<i>n</i> = 92, 30%) and B1 (87 = 29%). A total of nine <i>E. coli</i> isolates were confirmed as ESBL producers by double-disk synergy testing and multidrug resistant (MDR) to at least three antimicrobial drug classes. Using WGS, significantly higher numbers of ESBL-<i>E. coli</i> were detected in swine and dairy manure than from any other animal sources, suggesting that these may be the primary animal sources for ESBL producing <i>E. coli</i>. These isolates carry plasmids, such as IncFIA(B), IncFII, IncX1, IncX4, IncQ1, CollRNAI, Col440I, and acquired ARGs <i>aph</i>(6)-Id, <i>aph</i>(3″)-Ib, <i>aad</i>A5, <i>aph</i>(3′)-Ia, <i>bla</i>_CTX-M-15, <i>bla</i>_TEM-1B, <i>mph</i>A, <i>erm</i>B, <i>cat</i>A1, <i>sul</i>1, <i>sul</i>2, <i>tet</i>B, <i>dfr</i>A17. One of the <i>E. coli</i> isolates from swine with ST 410 was resistant to nine antibiotics and carried more than 28 virulence factors, and this ST has been shown to belong to an international high-risk clone. Our data suggests that ESBL producing <i>E. coli</i> are widely distributed in different animal sources, but swine and dairy cattle may be their main reservoir.