diff --git a/lib/matplotlib/backend_bases.py b/lib/matplotlib/backend_bases.py
index 2158990f578a..edb04edd59ee 100644
--- a/lib/matplotlib/backend_bases.py
+++ b/lib/matplotlib/backend_bases.py
@@ -1059,7 +1059,9 @@ def __init__(self, interval=None, callbacks=None):
             and `~.TimerBase.remove_callback` can be used.
         """
         self.callbacks = [] if callbacks is None else callbacks.copy()
-        # Set .interval and not ._interval to go through the property setter.
+        # Go through the property setters for validation and updates
+        self._interval = None
+        self._single = None
         self.interval = 1000 if interval is None else interval
         self.single_shot = False
 
@@ -1103,8 +1105,9 @@ def interval(self, interval):
         # milliseconds, and some error or give warnings.
         # Some backends also fail when interval == 0, so ensure >= 1 msec
         interval = max(int(interval), 1)
-        self._interval = interval
-        self._timer_set_interval()
+        if interval != self._interval:
+            self._interval = interval
+            self._timer_set_interval()
 
     @property
     def single_shot(self):
@@ -1113,8 +1116,9 @@ def single_shot(self):
 
     @single_shot.setter
     def single_shot(self, ss):
-        self._single = ss
-        self._timer_set_single_shot()
+        if ss != self._single:
+            self._single = ss
+            self._timer_set_single_shot()
 
     def add_callback(self, func, *args, **kwargs):
         """
@@ -2370,13 +2374,11 @@ def start_event_loop(self, timeout=0):
         """
         if timeout <= 0:
             timeout = np.inf
-        timestep = 0.01
-        counter = 0
+        t_end = time.perf_counter() + timeout
         self._looping = True
-        while self._looping and counter * timestep < timeout:
+        while self._looping and time.perf_counter() < t_end:
             self.flush_events()
-            time.sleep(timestep)
-            counter += 1
+            time.sleep(0.01)  # Pause for 10ms
 
     def stop_event_loop(self):
         """
diff --git a/lib/matplotlib/backends/_backend_tk.py b/lib/matplotlib/backends/_backend_tk.py
index 0bbff1379ffa..14f8a7b306a1 100644
--- a/lib/matplotlib/backends/_backend_tk.py
+++ b/lib/matplotlib/backends/_backend_tk.py
@@ -6,6 +6,7 @@
 import os.path
 import pathlib
 import sys
+import time
 import tkinter as tk
 import tkinter.filedialog
 import tkinter.font
@@ -126,12 +127,15 @@ class TimerTk(TimerBase):
 
     def __init__(self, parent, *args, **kwargs):
         self._timer = None
-        super().__init__(*args, **kwargs)
         self.parent = parent
+        super().__init__(*args, **kwargs)
 
     def _timer_start(self):
         self._timer_stop()
         self._timer = self.parent.after(self._interval, self._on_timer)
+        # Keep track of the firing time for repeating timers since
+        # we have to do this manually in Tk
+        self._timer_start_count = time.perf_counter_ns()
 
     def _timer_stop(self):
         if self._timer is not None:
@@ -139,6 +143,9 @@ def _timer_stop(self):
         self._timer = None
 
     def _on_timer(self):
+        # We want to measure the time spent in the callback, so we need to
+        # record the time before calling the base class method.
+        timer_fire_ms = (time.perf_counter_ns() - self._timer_start_count) // 1_000_000
         super()._on_timer()
         # Tk after() is only a single shot, so we need to add code here to
         # reset the timer if we're not operating in single shot mode.  However,
@@ -146,7 +153,20 @@ def _on_timer(self):
         # don't recreate the timer in that case.
         if not self._single and self._timer:
             if self._interval > 0:
-                self._timer = self.parent.after(self._interval, self._on_timer)
+                # We want to adjust our fire time independent of the time
+                # spent in the callback and not drift over time, so reference
+                # to the start count.
+                after_callback_ms = ((time.perf_counter_ns() - self._timer_start_count)
+                                     // 1_000_000)
+                if after_callback_ms - timer_fire_ms < self._interval:
+                    next_interval = self._interval - after_callback_ms % self._interval
+                    # minimum of 1ms
+                    next_interval = max(1, next_interval)
+                else:
+                    # Account for the callback being longer than the interval, where
+                    # we really want to fire the next timer as soon as possible.
+                    next_interval = 1
+                self._timer = self.parent.after(next_interval, self._on_timer)
             else:
                 # Edge case: Tcl after 0 *prepends* events to the queue
                 # so a 0 interval does not allow any other events to run.
@@ -158,6 +178,12 @@ def _on_timer(self):
         else:
             self._timer = None
 
+    def _timer_set_interval(self):
+        self._timer_start()
+
+    def _timer_set_single_shot(self):
+        self._timer_start()
+
 
 class FigureCanvasTk(FigureCanvasBase):
     required_interactive_framework = "tk"
diff --git a/lib/matplotlib/backends/backend_wx.py b/lib/matplotlib/backends/backend_wx.py
index f83a69d8361e..9eb054bf4089 100644
--- a/lib/matplotlib/backends/backend_wx.py
+++ b/lib/matplotlib/backends/backend_wx.py
@@ -69,6 +69,10 @@ def _timer_set_interval(self):
         if self._timer.IsRunning():
             self._timer_start()  # Restart with new interval.
 
+    def _timer_set_single_shot(self):
+        if self._timer.IsRunning():
+            self._timer_start()  # Restart with new interval.
+
 
 @_api.deprecated(
     "2.0", name="wx", obj_type="backend", removal="the future",
diff --git a/lib/matplotlib/tests/test_backend_bases.py b/lib/matplotlib/tests/test_backend_bases.py
index 0205eac42fb3..70e5c466d7fc 100644
--- a/lib/matplotlib/tests/test_backend_bases.py
+++ b/lib/matplotlib/tests/test_backend_bases.py
@@ -1,9 +1,10 @@
 import importlib
+from unittest.mock import patch
 
 from matplotlib import path, transforms
 from matplotlib.backend_bases import (
     FigureCanvasBase, KeyEvent, LocationEvent, MouseButton, MouseEvent,
-    NavigationToolbar2, RendererBase)
+    NavigationToolbar2, RendererBase, TimerBase)
 from matplotlib.backend_tools import RubberbandBase
 from matplotlib.figure import Figure
 from matplotlib.testing._markers import needs_pgf_xelatex
@@ -581,3 +582,31 @@ def test_interactive_pan_zoom_events(tool, button, patch_vis, forward_nav, t_s):
     # Check if twin-axes are properly triggered
     assert ax_t.get_xlim() == pytest.approx(ax_t_twin.get_xlim(), abs=0.15)
     assert ax_b.get_xlim() == pytest.approx(ax_b_twin.get_xlim(), abs=0.15)
+
+
+def test_timer_properties():
+    # Setting a property to the same value should not trigger the
+    # private setter call again.
+    timer = TimerBase(100)
+    with patch.object(timer, '_timer_set_interval') as mock:
+        timer.interval = 200
+        mock.assert_called_once()
+        assert timer.interval == 200
+        timer.interval = 200
+        # Make sure it wasn't called again
+        mock.assert_called_once()
+
+    with patch.object(timer, '_timer_set_single_shot') as mock:
+        timer.single_shot = True
+        mock.assert_called_once()
+        assert timer._single
+        timer.single_shot = True
+        # Make sure it wasn't called again
+        mock.assert_called_once()
+
+    # A timer with <1 millisecond gets converted to int and therefore 0
+    # milliseconds, which the mac framework interprets as singleshot.
+    # We only want singleshot if we specify that ourselves, otherwise we want
+    # a repeating timer, so make sure our interval is set to a minimum of 1ms.
+    timer.interval = 0.1
+    assert timer.interval == 1
diff --git a/lib/matplotlib/tests/test_backends_interactive.py b/lib/matplotlib/tests/test_backends_interactive.py
index a27783fa4be1..5a1ec29f387b 100644
--- a/lib/matplotlib/tests/test_backends_interactive.py
+++ b/lib/matplotlib/tests/test_backends_interactive.py
@@ -645,46 +645,79 @@ def test_fallback_to_different_backend():
 
 
 def _impl_test_interactive_timers():
-    # A timer with <1 millisecond gets converted to int and therefore 0
-    # milliseconds, which the mac framework interprets as singleshot.
-    # We only want singleshot if we specify that ourselves, otherwise we want
-    # a repeating timer
-    import os
+    # NOTE: We run the timer tests in parallel to avoid longer sequential
+    #       delays which adds to the testing time. Add new tests to one of
+    #       the current event loop iterations if possible.
+    import time
     from unittest.mock import Mock
     import matplotlib.pyplot as plt
-    # increase pause duration on CI to let things spin up
-    # particularly relevant for gtk3cairo
-    pause_time = 2 if os.getenv("CI") else 0.5
-    fig = plt.figure()
-    plt.pause(pause_time)
-    timer = fig.canvas.new_timer(0.1)
-    mock = Mock()
-    timer.add_callback(mock)
-    timer.start()
-    plt.pause(pause_time)
-    timer.stop()
-    assert mock.call_count > 1
-
-    # Now turn it into a single shot timer and verify only one gets triggered
-    mock.call_count = 0
-    timer.single_shot = True
-    timer.start()
-    plt.pause(pause_time)
-    assert mock.call_count == 1
 
-    # Make sure we can start the timer a second time
-    timer.start()
-    plt.pause(pause_time)
-    assert mock.call_count == 2
-    plt.close("all")
+    fig = plt.figure()
+    # Start at 2s interval (wouldn't get any firings), then update to 100ms
+    timer_repeating = fig.canvas.new_timer(2000)
+    mock_repeating = Mock()
+    timer_repeating.add_callback(mock_repeating)
+
+    timer_single_shot = fig.canvas.new_timer(100)
+    mock_single_shot = Mock()
+    timer_single_shot.add_callback(mock_single_shot)
+
+    timer_repeating.start()
+    # Test updating the interval updates a running timer
+    timer_repeating.interval = 100
+    # Start as a repeating timer then change to singleshot via the attribute
+    timer_single_shot.start()
+    timer_single_shot.single_shot = True
+
+    fig.canvas.start_event_loop(0.5)
+    assert 2 <= mock_repeating.call_count <= 5, \
+        f"Interval update: Expected 2-5 calls, got {mock_repeating.call_count}"
+    assert mock_single_shot.call_count == 1, \
+        f"Singleshot: Expected 1 call, got {mock_single_shot.call_count}"
+
+    # 500ms timer triggers and the callback takes 400ms to run
+    # Test that we don't drift and that we get called on every 500ms
+    # firing and not every 900ms
+    timer_repeating.interval = 500
+    # sleep for 80% of the interval
+    sleep_time = timer_repeating.interval / 1000 * 0.8
+    mock_repeating.side_effect = lambda: time.sleep(sleep_time)
+    # calling start() again on a repeating timer should remove the old
+    # one, so we don't want double the number of calls here either because
+    # two timers are potentially running.
+    timer_repeating.start()
+    mock_repeating.call_count = 0
+    # Make sure we can start the timer after stopping a singleshot timer
+    timer_single_shot.stop()
+    timer_single_shot.start()
+
+    # CI resources are inconsistent, so we need to allow for some slop
+    event_loop_time = 10 if os.getenv("CI") else 3  # in seconds
+    expected_calls = int(event_loop_time / (timer_repeating.interval / 1000))
+
+    t_start = time.perf_counter()
+    fig.canvas.start_event_loop(event_loop_time)
+    t_loop = time.perf_counter() - t_start
+    # Should be around event_loop_time, but allow for some slop on CI.
+    # We want to make sure we aren't getting
+    # event_loop_time + (callback time)*niterations
+    assert event_loop_time * 0.95 < t_loop < event_loop_time / 0.7, \
+        f"Event loop: Expected to run for around {event_loop_time}s, " \
+        f"but ran for {t_loop:.2f}s"
+    # Not exact timers, so add some slop. (Quite a bit for CI resources)
+    assert abs(mock_repeating.call_count - expected_calls) / expected_calls <= 0.3, \
+        f"Slow callback: Expected {expected_calls} calls, " \
+        f"got {mock_repeating.call_count}"
+    assert mock_single_shot.call_count == 2, \
+        f"Singleshot: Expected 2 calls, got {mock_single_shot.call_count}"
 
 
 @pytest.mark.parametrize("env", _get_testable_interactive_backends())
 def test_interactive_timers(env):
-    if env["MPLBACKEND"] == "gtk3cairo" and os.getenv("CI"):
-        pytest.skip("gtk3cairo timers do not work in remote CI")
     if env["MPLBACKEND"] == "wx":
         pytest.skip("wx backend is deprecated; tests failed on appveyor")
+    if env["MPLBACKEND"].startswith("gtk3") and is_ci_environment():
+        pytest.xfail("GTK3 backend timer is slow on CI resources")
     _run_helper(_impl_test_interactive_timers,
                 timeout=_test_timeout, extra_env=env)
 
diff --git a/src/_macosx.m b/src/_macosx.m
index aa2a6e68cda5..d7396e4b43f2 100755
--- a/src/_macosx.m
+++ b/src/_macosx.m
@@ -1754,6 +1754,15 @@ - (void)flagsChanged:(NSEvent *)event
                                (void*) self, (void*)(self->timer));
 }
 
+static void
+Timer__timer_stop_impl(Timer* self)
+{
+    if (self->timer) {
+        [self->timer invalidate];
+        self->timer = NULL;
+    }
+}
+
 static PyObject*
 Timer__timer_start(Timer* self, PyObject* args)
 {
@@ -1772,20 +1781,21 @@ - (void)flagsChanged:(NSEvent *)event
         goto exit;
     }
 
+    // Stop the current timer if it is already running
+    Timer__timer_stop_impl(self);
     // hold a reference to the timer so we can invalidate/stop it later
-    self->timer = [NSTimer timerWithTimeInterval: interval
-                                         repeats: !single
-                                           block: ^(NSTimer *timer) {
-        gil_call_method((PyObject*)self, "_on_timer");
-        if (single) {
-            // A single-shot timer will be automatically invalidated when it fires, so
-            // we shouldn't do it ourselves when the object is deleted.
-            self->timer = NULL;
-        }
+    self->timer = [NSTimer scheduledTimerWithTimeInterval: interval
+                                                  repeats: !single
+                                                    block: ^(NSTimer *timer) {
+        dispatch_async(dispatch_get_main_queue(), ^{
+            gil_call_method((PyObject*)self, "_on_timer");
+            if (single) {
+                // A single-shot timer will be automatically invalidated when it fires, so
+                // we shouldn't do it ourselves when the object is deleted.
+                self->timer = NULL;
+            }
+        });
     }];
-    // Schedule the timer on the main run loop which is needed
-    // when updating the UI from a background thread
-    [[NSRunLoop mainRunLoop] addTimer: self->timer forMode: NSRunLoopCommonModes];
 
 exit:
     Py_XDECREF(py_interval);
@@ -1798,19 +1808,22 @@ - (void)flagsChanged:(NSEvent *)event
     }
 }
 
-static void
-Timer__timer_stop_impl(Timer* self)
+static PyObject*
+Timer__timer_stop(Timer* self)
 {
-    if (self->timer) {
-        [self->timer invalidate];
-        self->timer = NULL;
-    }
+    Timer__timer_stop_impl(self);
+    Py_RETURN_NONE;
 }
 
 static PyObject*
-Timer__timer_stop(Timer* self)
+Timer__timer_update(Timer* self)
 {
-    Timer__timer_stop_impl(self);
+    // stop and invalidate a timer if it is already running and then create a new one
+    // where the start() method retrieves the updated interval internally
+    if (self->timer) {
+        Timer__timer_stop_impl(self);
+        gil_call_method((PyObject*)self, "_timer_start");
+    }
     Py_RETURN_NONE;
 }
 
@@ -1840,6 +1853,12 @@ - (void)flagsChanged:(NSEvent *)event
         {"_timer_stop",
          (PyCFunction)Timer__timer_stop,
          METH_NOARGS},
+        {"_timer_set_interval",
+         (PyCFunction)Timer__timer_update,
+         METH_NOARGS},
+        {"_timer_set_single_shot",
+         (PyCFunction)Timer__timer_update,
+         METH_NOARGS},
         {}  // sentinel
     },
 };