Yippee, problem solved. Because the PWM signal was being turned on by an asynchronous signal (whatever the loop time happens to be), sometimes the counter value would be such that the first pulse would be extra long. By resetting Timer1 before I turn on PWM with analogWrite, I never get the extra long first pulse.
PWM volume control
Low frequency signal turns on high frequency PWM
int Outpin = 9; //TP4
long ontime = 5; //sets the ontime to half a cycle at 100Hz
int DutyCycle = 25; //duty cycle of 25/255 for testing.
TCCR1B = TCCR1B & 0b11111000|0b1; //raising the PWM frequency to about 32kHz
TCNT1=0; //Resets the counter in Timer1 to zero each time
delay(ontime); //"off" time equal to "on" time for testing