Background: HGT1 NMI tumors have a 40% risk of R and 21% risk of P. Distinguishing aggressive versus indolent HGT1 disease is critical to decide which patients will benefit from early cystectomy. We examined genetic features associated with recurrence and progression. Methods: FFPE tumor/normal (T/N) samples were available from a clinically annotated cohort with HGT1 (7.4 y f/u), who were managed in a uniform manner using TURB and BCG. Clinical outcome was classified as: non-recurrent disease < 4 years (good outcome, GO), recurrent (R), or progression to MI or M1 (PD). 37 primary T/N matched sample pairs were subject to WES followed by Broad standard analysis pipelines, yielding 27 QC-passed T/N pairs (exome coverage > 23 Mb). Results: TP53 mutations (8/27) were most common in PD samples (2-R/ 6-PD, P = 0.009 by Fisher's test, FDR = 0.2) while RB1 mutations (6/27) were enriched in GO samples (5-GO/ 1-PD, P = 0.024, FDR = 0.24). Other recurrent mutations not enriched by clinical subtype ( > 4) included ERBB3, KDM6A, STAG2, and KMT2C. Three mutational signatures were identified from single nucleotide variants: APOBEC (67%), C > T at CpG (4%), COSMIC-5 (unknown origin) (29%). The COSMIC-5 signature was enriched in GO samples (P = 0.03 by Mann-Whitney between GO vs PD+R (median 32% vs 4%). The sample with highest mutation-rate had more than 80% COSMIC-5 signature mutations, and an ERCC2 S246Y mutation. Two most common focal copy number events were CDKN2A deletions (2-GO/3-R/4-PD) and 1q23 amplification (AMP) spanning MCL1 (2-GO/4-R/2-PD) and PVRL4 (1-GO/3-R/3-PD). Recurrent focal AMP ( > 4 samples) also included MDM2(3-GO/2-R/1-PD), CCNE1 (3-R/2-PD), YWHAZ (1-GO/1-R/2-PD), and ERBB2 (2-GO/1-R/1-PD). Combined AMPs in E2F3/CCND1/CCNE1 were enriched in PD or R samples (5-R/4-PD, P = 0.01 Fisher's test, FDR = 0.14) and co-occurred with TP53 mutation (6 of 8 TP53 mutations, P = 0.006, FDR = 0.12). Conclusions: Analysis of mutations and copy number alterations in HGT1 bladder tumors may improve prediction of good outcome vs. recurrence or progression, enabling a management strategy of early cystectomy for those with poor prognosis, and continued observation for those with predicted good outcome.