diff --git a/include/wx/msw/listctrl.h b/include/wx/msw/listctrl.h
index 042e8348e6..4bad3f375f 100644
--- a/include/wx/msw/listctrl.h
+++ b/include/wx/msw/listctrl.h
@@ -481,6 +481,9 @@ private:
     // another WM_SIZE to be generated.
     int m_inResize = 0;
 
+    // Non-zero while the native control is auto-sizing a column, which it does
+    // by sending NM_CUSTOMDRAW notifications for all of its items.
+    int m_inAutoSize = 0;
 
     wxDECLARE_DYNAMIC_CLASS(wxListCtrl);
     wxDECLARE_EVENT_TABLE();
diff --git a/src/msw/listctrl.cpp b/src/msw/listctrl.cpp
index 5a5422db45..233d35f8c1 100644
--- a/src/msw/listctrl.cpp
+++ b/src/msw/listctrl.cpp
@@ -843,7 +843,18 @@ bool wxListCtrl::SetColumnWidth(int col, int width)
         return true;
     }
 
-    if ( !ListView_SetColumnWidth(GetHwnd(), col, width) )
+    // See the comment in OnCustomDraw() for why we need to know about this.
+    const bool autoSize = width == LVSCW_AUTOSIZE ||
+                            width == LVSCW_AUTOSIZE_USEHEADER;
+    if ( autoSize )
+        m_inAutoSize++;
+
+    const bool ok = ListView_SetColumnWidth(GetHwnd(), col, width) != FALSE;
+
+    if ( autoSize )
+        m_inAutoSize--;
+
+    if ( !ok )
         return false;
 
     // Failure to explicitly refresh the control with horizontal rules results
@@ -3540,7 +3551,11 @@ WXLPARAM wxListCtrl::OnCustomDraw(WXLPARAM lParam)
             //
             // for virtual controls, always suppose that we have attributes as
             // there is no way to check for this
-            if ( IsVirtual() || m_hasAnyAttr || wxMSWDarkMode::IsActive() )
+            //
+            // in dark mode we also need to draw all items ourselves, but not
+            // when auto-sizing the columns, see CDDS_ITEMPREPAINT case below
+            if ( IsVirtual() || m_hasAnyAttr ||
+                    (wxMSWDarkMode::IsActive() && !m_inAutoSize) )
                 return CDRF_NOTIFYITEMDRAW;
             break;
 
@@ -3552,7 +3567,15 @@ WXLPARAM wxListCtrl::OnCustomDraw(WXLPARAM lParam)
             // repeat the same drawing once per column, which is not only
             // wasteful but also results in visible delays when scrolling
             // lists with many columns.
-            if ( wxMSWDarkMode::IsActive() && InReportView() )
+            //
+            // Don't do it while auto-sizing a column however: in this case the
+            // native control sends us this notification for every item, but
+            // only to allow us to select a different font for measuring it, so
+            // painting the entire row here would be useless and would make
+            // setting the column width very slow for big controls (see
+            // #24011). Just fall through to the default handling below, which
+            // takes care of the custom fonts, if any, instead.
+            if ( wxMSWDarkMode::IsActive() && InReportView() && !m_inAutoSize )
             {
                 const int item = nmcd.dwItemSpec;