diff --git a/autoload/airline/extensions/tabline/tabs.vim b/autoload/airline/extensions/tabline/tabs.vim
index 80a8a0a..c822e1d 100644
--- a/autoload/airline/extensions/tabline/tabs.vim
+++ b/autoload/airline/extensions/tabline/tabs.vim
@@ -103,12 +103,20 @@ function! airline#extensions#tabline#tabs#get()
   let right_position = tabs_position + 1
   let remaining_space = &columns - s:strchars(s:evaluate_tabline(b.build()))
 
+  let left_sep_size = s:strchars(s:evaluate_tabline(b._context.left_sep))
+  let left_alt_sep_size = s:strchars(s:evaluate_tabline(b._context.left_alt_sep))
+
   let skipped_tabs_marker = get(g:, 'airline#extensions#tabline#overflow_marker', g:airline_symbols.ellipsis)
-  let remaining_space -= 2 * s:strchars(s:evaluate_tabline(skipped_tabs_marker))
+  let skipped_tabs_marker_size = s:strchars(s:evaluate_tabline(skipped_tabs_marker))
+  " The left marker will have left_alt_sep, and the right will have left_sep.
+  let remaining_space -= 2 * skipped_tabs_marker_size + left_sep_size + left_alt_sep_size
 
   " Add the current tab
   let tab_title = s:get_title(tab_nr_type, curtab)
-  let remaining_space -= s:strchars(s:evaluate_tabline(tab_title)) + 1
+  let remaining_space -= s:strchars(s:evaluate_tabline(tab_title))
+  " There are always two left_seps (either side of the selected tab) and all
+  " other seperators are left_alt_seps.
+  let remaining_space -= 2 * left_sep_size - left_alt_sep_size
   let group = 'airline_tabsel'
   if g:airline_detect_modified
     for bi in tabpagebuflist(curtab)
@@ -128,7 +136,7 @@ function! airline#extensions#tabline#tabs#get()
   " Add the tab to the right
   if right_tab <= num_tabs
     let tab_title = s:get_title(tab_nr_type, right_tab)
-    let remaining_space -= s:strchars(s:evaluate_tabline(tab_title)) + 1
+    let remaining_space -= s:strchars(s:evaluate_tabline(tab_title)) + left_alt_sep_size
     call b.insert_section('airline_tab', tab_title, right_position)
     let right_position += 1
     let right_tab += 1
@@ -137,7 +145,7 @@ function! airline#extensions#tabline#tabs#get()
   while remaining_space > 0
     if left_tab > 0
       let tab_title = s:get_title(tab_nr_type, left_tab)
-      let remaining_space -= s:strchars(s:evaluate_tabline(tab_title)) + 1
+      let remaining_space -= s:strchars(s:evaluate_tabline(tab_title)) + left_alt_sep_size
       if remaining_space >= 0
         call b.insert_section('airline_tab', tab_title, left_position)
         let right_position += 1
@@ -145,7 +153,7 @@ function! airline#extensions#tabline#tabs#get()
       endif
     elseif right_tab <= num_tabs
       let tab_title = s:get_title(tab_nr_type, right_tab)
-      let remaining_space -= s:strchars(s:evaluate_tabline(tab_title)) + 1
+      let remaining_space -= s:strchars(s:evaluate_tabline(tab_title)) + left_alt_sep_size
       if remaining_space >= 0
         call b.insert_section('airline_tab', tab_title, right_position)
         let right_position += 1